diff --git a/pkg/setting/setting.go b/pkg/setting/setting.go
index 21f43269fc9..e31ceae24aa 100644
--- a/pkg/setting/setting.go
+++ b/pkg/setting/setting.go
@@ -575,13 +575,14 @@ type Cfg struct {
 	MaxPageSizeBytes                           int
 	IndexPath                                  string
 	IndexWorkers                               int
+	IndexRebuildWorkers                        int
 	IndexMaxBatchSize                          int
 	IndexFileThreshold                         int
 	IndexMinCount                              int
 	IndexRebuildInterval                       time.Duration
 	IndexCacheTTL                              time.Duration
-	MaxFileIndexAge                            time.Duration // Max age of file-based indexes. Index older than this will not be reused between restarts.
-	MinFileIndexBuildVersion                   string        // Minimum version of Grafana that built the file-based index. If index was built with older Grafana, it will not be reused between restarts.
+	MaxFileIndexAge                            time.Duration // Max age of file-based indexes. Index older than this will be rebuilt asynchronously.
+	MinFileIndexBuildVersion                   string        // Minimum version of Grafana that built the file-based index. If index was built with older Grafana, it will be rebuilt asynchronously.
 	EnableSharding                             bool
 	QOSEnabled                                 bool
 	QOSNumberWorker                            int
diff --git a/pkg/setting/setting_unified_storage.go b/pkg/setting/setting_unified_storage.go
index 921fb2f24a5..0ebb6c93830 100644
--- a/pkg/setting/setting_unified_storage.go
+++ b/pkg/setting/setting_unified_storage.go
@@ -54,6 +54,7 @@ func (cfg *Cfg) setUnifiedStorageConfig() {
 	cfg.MaxPageSizeBytes = section.Key("max_page_size_bytes").MustInt(0)
 	cfg.IndexPath = section.Key("index_path").String()
 	cfg.IndexWorkers = section.Key("index_workers").MustInt(10)
+	cfg.IndexRebuildWorkers = section.Key("index_rebuild_workers").MustInt(5)
 	cfg.IndexMaxBatchSize = section.Key("index_max_batch_size").MustInt(100)
 	cfg.EnableSharding = section.Key("enable_sharding").MustBool(false)
 	cfg.QOSEnabled = section.Key("qos_enabled").MustBool(false)
diff --git a/pkg/storage/unified/resource/bleve_index_metrics.go b/pkg/storage/unified/resource/bleve_index_metrics.go
index bdd3f071232..00e08c62389 100644
--- a/pkg/storage/unified/resource/bleve_index_metrics.go
+++ b/pkg/storage/unified/resource/bleve_index_metrics.go
@@ -20,6 +20,7 @@ type BleveIndexMetrics struct {
 	UpdateLatency        prometheus.Histogram
 	UpdatedDocuments     prometheus.Summary
 	SearchUpdateWaitTime *prometheus.HistogramVec
+	RebuildQueueLength   prometheus.Gauge
 }
 
 var IndexCreationBuckets = []float64{1, 5, 10, 25, 50, 75, 100, 200, 300, 400, 500, 600, 700, 800, 900, 1000}
@@ -84,6 +85,10 @@ func ProvideIndexMetrics(reg prometheus.Registerer) *BleveIndexMetrics {
 			NativeHistogramMaxBucketNumber:  160,
 			NativeHistogramMinResetDuration: time.Hour,
 		}, []string{"reason"}),
+		RebuildQueueLength: promauto.With(reg).NewGauge(prometheus.GaugeOpts{
+			Name: "index_server_rebuild_queue_length",
+			Help: "Number of indexes waiting for rebuild",
+		}),
 	}
 
 	// Initialize labels.
diff --git a/pkg/storage/unified/resource/search.go b/pkg/storage/unified/resource/search.go
index fbf70eebe4f..bc85a0a5a8a 100644
--- a/pkg/storage/unified/resource/search.go
+++ b/pkg/storage/unified/resource/search.go
@@ -10,6 +10,7 @@ import (
 	"sync"
 	"time"
 
+	"github.com/Masterminds/semver"
 	"github.com/hashicorp/golang-lru/v2/expirable"
 	"go.opentelemetry.io/otel/attribute"
 	"go.opentelemetry.io/otel/trace"
@@ -24,6 +25,7 @@ import (
 	folders "github.com/grafana/grafana/apps/folder/pkg/apis/folder/v1beta1"
 	"github.com/grafana/grafana/pkg/infra/tracing"
 	"github.com/grafana/grafana/pkg/storage/unified/resourcepb"
+	"github.com/grafana/grafana/pkg/util/debouncer"
 )
 
 const maxBatchSize = 1000
@@ -61,6 +63,11 @@ type BulkIndexRequest struct {
 	ResourceVersion int64
 }
 
+type IndexBuildInfo struct {
+	BuildTime    time.Time       // Timestamp when the index was built. This value doesn't change on subsequent index updates.
+	BuildVersion *semver.Version // Grafana version used when originally building the index. This value doesn't change on subsequent index updates.
+}
+
 type ResourceIndex interface {
 	// BulkIndex allows for multiple index actions to be performed in a single call.
 	// The order of the items is guaranteed to be the same as the input
@@ -82,6 +89,9 @@ type ResourceIndex interface {
 	// UpdateIndex updates the index with the latest data (using update function provided when index was built) to guarantee strong consistency during the search.
 	// Returns RV to which index was updated.
 	UpdateIndex(ctx context.Context, reason string) (int64, error)
+
+	// BuildInfo returns build information about the index.
+	BuildInfo() (IndexBuildInfo, error)
 }
 
 type BuildFn func(index ResourceIndex) (int64, error)
@@ -112,6 +122,9 @@ type SearchBackend interface {
 
 	// TotalDocs returns the total number of documents across all indexes.
 	TotalDocs() int64
+
+	// GetOpenIndexes returns the list of indexes that are currently open.
+	GetOpenIndexes() []NamespacedResource
 }
 
 const tracingPrexfixSearch = "unified_search."
@@ -132,8 +145,17 @@ type searchSupport struct {
 
 	buildIndex singleflight.Group
 
-	// periodic rebuilding of the indexes to keep usage insights up to date
-	rebuildInterval time.Duration
+	// since usage insights is not in unified storage, we need to periodically rebuild the index
+	// to make sure these data points are up to date.
+	dashboardIndexMaxAge time.Duration
+	maxIndexAge          time.Duration
+	minBuildVersion      *semver.Version
+
+	bgTaskWg     sync.WaitGroup
+	bgTaskCancel func()
+
+	rebuildQueue   *debouncer.Queue[rebuildRequest]
+	rebuildWorkers int
 }
 
 var (
@@ -150,8 +172,12 @@ func newSearchSupport(opts SearchOptions, storage StorageBackend, access types.A
 		return nil, fmt.Errorf("missing tracer")
 	}
 
-	if opts.WorkerThreads < 1 {
-		opts.WorkerThreads = 1
+	if opts.InitWorkerThreads < 1 {
+		opts.InitWorkerThreads = 1
+	}
+
+	if opts.IndexRebuildWorkers < 1 {
+		opts.IndexRebuildWorkers = 1
 	}
 
 	if ownsIndexFn == nil {
@@ -161,18 +187,24 @@ func newSearchSupport(opts SearchOptions, storage StorageBackend, access types.A
 	}
 
 	support = &searchSupport{
-		access:          access,
-		tracer:          tracer,
-		storage:         storage,
-		search:          opts.Backend,
-		log:             slog.Default().With("logger", "resource-search"),
-		initWorkers:     opts.WorkerThreads,
-		initMinSize:     opts.InitMinCount,
-		indexMetrics:    indexMetrics,
-		rebuildInterval: opts.RebuildInterval,
-		ownsIndexFn:     ownsIndexFn,
+		access:         access,
+		tracer:         tracer,
+		storage:        storage,
+		search:         opts.Backend,
+		log:            slog.Default().With("logger", "resource-search"),
+		initWorkers:    opts.InitWorkerThreads,
+		rebuildWorkers: opts.IndexRebuildWorkers,
+		initMinSize:    opts.InitMinCount,
+		indexMetrics:   indexMetrics,
+		ownsIndexFn:    ownsIndexFn,
+
+		dashboardIndexMaxAge: opts.DashboardIndexMaxAge,
+		maxIndexAge:          opts.MaxIndexAge,
+		minBuildVersion:      opts.MinBuildVersion,
 	}
 
+	support.rebuildQueue = debouncer.NewQueue(combineRebuildRequests)
+
 	info, err := opts.Resources.GetDocumentBuilders()
 	if err != nil {
 		return nil, err
@@ -186,6 +218,27 @@ func newSearchSupport(opts SearchOptions, storage StorageBackend, access types.A
 	return support, err
 }
 
+func combineRebuildRequests(a, b rebuildRequest) (c rebuildRequest, ok bool) {
+	if a.NamespacedResource != b.NamespacedResource {
+		// We can only combine requests for the same keys.
+		return rebuildRequest{}, false
+	}
+
+	ret := a
+
+	// Using higher "min build version" is stricter condition, and causes more indexes to be rebuilt.
+	if a.minBuildVersion == nil || (b.minBuildVersion != nil && b.minBuildVersion.GreaterThan(a.minBuildVersion)) {
+		ret.minBuildVersion = b.minBuildVersion
+	}
+
+	// Using higher "min build time" is stricter condition, and causes more indexes to be rebuilt.
+	if a.minBuildTime.IsZero() || (!b.minBuildTime.IsZero() && b.minBuildTime.After(a.minBuildTime)) {
+		ret.minBuildTime = b.minBuildTime
+	}
+
+	return ret, true
+}
+
 func (s *searchSupport) ListManagedObjects(ctx context.Context, req *resourcepb.ListManagedObjectsRequest) (*resourcepb.ListManagedObjectsResponse, error) {
 	if req.NextPageToken != "" {
 		return &resourcepb.ListManagedObjectsResponse{
@@ -401,7 +454,7 @@ func (s *searchSupport) GetStats(ctx context.Context, req *resourcepb.ResourceSt
 	return rsp, nil
 }
 
-func (s *searchSupport) buildIndexes(ctx context.Context, rebuild bool) (int, error) {
+func (s *searchSupport) buildIndexes(ctx context.Context) (int, error) {
 	totalBatchesIndexed := 0
 	group := errgroup.Group{}
 	group.SetLimit(s.initWorkers)
@@ -412,11 +465,6 @@ func (s *searchSupport) buildIndexes(ctx context.Context, rebuild bool) (int, er
 	}
 
 	for _, info := range stats {
-		// only periodically rebuild the dashboard index, specifically to update the usage insights data
-		if rebuild && info.Resource != dashboardv1.DASHBOARD_RESOURCE {
-			continue
-		}
-
 		own, err := s.ownsIndexFn(info.NamespacedResource)
 		if err != nil {
 			s.log.Warn("failed to check index ownership, building index", "namespace", info.Namespace, "group", info.Group, "resource", info.Resource, "error", err)
@@ -426,18 +474,11 @@ func (s *searchSupport) buildIndexes(ctx context.Context, rebuild bool) (int, er
 		}
 
 		group.Go(func() error {
-			if rebuild {
-				// we need to clear the cache to make sure we get the latest usage insights data
-				s.builders.clearNamespacedCache(info.NamespacedResource)
-			}
 			totalBatchesIndexed++
 
-			s.log.Debug("building index", "namespace", info.Namespace, "group", info.Group, "resource", info.Resource, "rebuild", rebuild)
+			s.log.Debug("building index", "namespace", info.Namespace, "group", info.Group, "resource", info.Resource)
 			reason := "init"
-			if rebuild {
-				reason = "rebuild"
-			}
-			_, err := s.build(ctx, info.NamespacedResource, info.Count, reason, rebuild)
+			_, err := s.build(ctx, info.NamespacedResource, info.Count, reason, false)
 			return err
 		})
 	}
@@ -457,30 +498,41 @@ func (s *searchSupport) init(ctx context.Context) error {
 	defer span.End()
 	start := time.Now().Unix()
 
-	totalBatchesIndexed, err := s.buildIndexes(ctx, false)
+	totalBatchesIndexed, err := s.buildIndexes(ctx)
 	if err != nil {
 		return err
 	}
 
 	span.AddEvent("namespaces indexed", trace.WithAttributes(attribute.Int("namespaced_indexed", totalBatchesIndexed)))
 
-	// since usage insights is not in unified storage, we need to periodically rebuild the index
-	// to make sure these data points are up to date.
-	if s.rebuildInterval > 0 {
-		go s.startPeriodicRebuild(origCtx)
+	subctx, cancel := context.WithCancel(origCtx)
+
+	s.bgTaskCancel = cancel
+	for i := 0; i < s.rebuildWorkers; i++ {
+		s.bgTaskWg.Add(1)
+		go s.runIndexRebuilder(subctx)
 	}
 
+	s.bgTaskWg.Add(1)
+	go s.runPeriodicScanForIndexesToRebuild(subctx)
+
 	end := time.Now().Unix()
 	s.log.Info("search index initialized", "duration_secs", end-start, "total_docs", s.search.TotalDocs())
 
 	return nil
 }
 
-func (s *searchSupport) startPeriodicRebuild(ctx context.Context) {
-	ticker := time.NewTicker(s.rebuildInterval)
-	defer ticker.Stop()
+func (s *searchSupport) stop() {
+	// Stop background tasks.
+	s.bgTaskCancel()
+	s.bgTaskWg.Wait()
+}
 
-	s.log.Info("starting periodic index rebuild", "interval", s.rebuildInterval)
+func (s *searchSupport) runPeriodicScanForIndexesToRebuild(ctx context.Context) {
+	defer s.bgTaskWg.Done()
+
+	ticker := time.NewTicker(5 * time.Minute)
+	defer ticker.Stop()
 
 	for {
 		select {
@@ -488,35 +540,166 @@ func (s *searchSupport) startPeriodicRebuild(ctx context.Context) {
 			s.log.Info("stopping periodic index rebuild due to context cancellation")
 			return
 		case <-ticker.C:
-			s.log.Info("starting periodic index rebuild")
-			if err := s.rebuildDashboardIndexes(ctx); err != nil {
-				s.log.Error("error during periodic index rebuild", "error", err)
-			} else {
-				s.log.Info("periodic index rebuild completed successfully")
+			s.findIndexesToRebuild(ctx, time.Now())
+		}
+	}
+}
+
+func (s *searchSupport) findIndexesToRebuild(ctx context.Context, now time.Time) {
+	// Check all open indexes and see if any of them need to be rebuilt.
+	// This is done periodically to make sure that the indexes are up to date.
+
+	keys := s.search.GetOpenIndexes()
+	for _, key := range keys {
+		idx, err := s.search.GetIndex(ctx, key)
+		if err != nil {
+			s.log.Error("failed to check index to rebuild", "key", key, "error", err)
+			continue
+		}
+
+		if idx == nil {
+			// This can happen if index was closed in the meantime.
+			continue
+		}
+
+		maxAge := s.maxIndexAge
+		if key.Resource == dashboardv1.DASHBOARD_RESOURCE {
+			maxAge = s.dashboardIndexMaxAge
+		}
+
+		var minBuildTime time.Time
+		if maxAge > 0 {
+			minBuildTime = now.Add(-maxAge)
+		}
+
+		bi, err := idx.BuildInfo()
+		if err != nil {
+			s.log.Error("failed to get build info for index to rebuild", "key", key, "error", err)
+			continue
+		}
+
+		if shouldRebuildIndex(s.minBuildVersion, bi, minBuildTime, nil) {
+			s.rebuildQueue.Add(rebuildRequest{
+				NamespacedResource: key,
+				minBuildTime:       minBuildTime,
+				minBuildVersion:    s.minBuildVersion,
+			})
+
+			if s.indexMetrics != nil {
+				s.indexMetrics.RebuildQueueLength.Set(float64(s.rebuildQueue.Len()))
 			}
 		}
 	}
 }
 
-func (s *searchSupport) rebuildDashboardIndexes(ctx context.Context) error {
-	ctx, span := s.tracer.Start(ctx, tracingPrexfixSearch+"RebuildDashboardIndexes")
+// runIndexRebuilder is a goroutine waiting for rebuild requests, and rebuilds indexes specified in those requests.
+// Rebuild requests can be generated periodically (if configured), or after new documents have been imported into the storage with old RVs.
+func (s *searchSupport) runIndexRebuilder(ctx context.Context) {
+	defer s.bgTaskWg.Done()
+
+	for {
+		req, err := s.rebuildQueue.Next(ctx)
+		if err != nil {
+			s.log.Info("index rebuilder stopped", "error", err)
+			return
+		}
+
+		if s.indexMetrics != nil {
+			s.indexMetrics.RebuildQueueLength.Set(float64(s.rebuildQueue.Len()))
+		}
+
+		s.rebuildIndex(ctx, req)
+	}
+}
+
+func (s *searchSupport) rebuildIndex(ctx context.Context, req rebuildRequest) {
+	ctx, span := s.tracer.Start(ctx, tracingPrexfixSearch+"RebuildIndex")
 	defer span.End()
 
-	start := time.Now()
-	s.log.Info("rebuilding all search indexes")
+	l := s.log.With("namespace", req.Namespace, "group", req.Group, "resource", req.Resource)
 
-	totalBatchesIndexed, err := s.buildIndexes(ctx, true)
+	idx, err := s.search.GetIndex(ctx, req.NamespacedResource)
 	if err != nil {
-		return fmt.Errorf("failed to rebuild dashboard indexes: %w", err)
+		span.RecordError(err)
+		l.Error("failed to get index to rebuild", "error", err)
+		return
 	}
 
-	end := time.Now()
-	duration := end.Sub(start)
-	s.log.Info("completed rebuilding all dashboard search indexes",
-		"duration", duration,
-		"rebuilt_indexes", totalBatchesIndexed,
-		"total_docs", s.search.TotalDocs())
-	return nil
+	if idx == nil {
+		span.AddEvent("index not found")
+		l.Error("index not found")
+		return
+	}
+
+	bi, err := idx.BuildInfo()
+	if err != nil {
+		span.RecordError(err)
+		l.Error("failed to get build info for index to rebuild", "error", err)
+	}
+
+	rebuild := shouldRebuildIndex(req.minBuildVersion, bi, req.minBuildTime, l)
+	if !rebuild {
+		span.AddEvent("index not rebuilt")
+		l.Info("index doesn't need to be rebuilt")
+		return
+	}
+
+	if req.Resource == dashboardv1.DASHBOARD_RESOURCE {
+		// we need to clear the cache to make sure we get the latest usage insights data
+		s.builders.clearNamespacedCache(req.NamespacedResource)
+	}
+
+	// Get the correct value of size + RV for building the index. This is important for our Bleve
+	// backend to decide whether to build index in-memory or as file-based.
+	stats, err := s.storage.GetResourceStats(ctx, req.Namespace, 0)
+	if err != nil {
+		span.RecordError(fmt.Errorf("failed to get resource stats: %w", err))
+		l.Error("failed to get resource stats", "error", err)
+		return
+	}
+
+	size := int64(0)
+	for _, stat := range stats {
+		if stat.Namespace == req.Namespace && stat.Group == req.Group && stat.Resource == req.Resource {
+			size = stat.Count
+			break
+		}
+	}
+
+	_, err = s.build(ctx, req.NamespacedResource, size, "rebuild", true)
+	if err != nil {
+		span.RecordError(err)
+		l.Error("failed to rebuild index", "error", err)
+	}
+}
+
+func shouldRebuildIndex(minBuildVersion *semver.Version, buildInfo IndexBuildInfo, minBuildTime time.Time, rebuildLogger *slog.Logger) bool {
+	if !minBuildTime.IsZero() {
+		if buildInfo.BuildTime.IsZero() || buildInfo.BuildTime.Before(minBuildTime) {
+			if rebuildLogger != nil {
+				rebuildLogger.Info("index build time is before minBuildTime, rebuilding the index", "indexBuildTime", buildInfo.BuildTime, "minBuildTime", minBuildTime)
+			}
+			return true
+		}
+	}
+
+	if minBuildVersion != nil {
+		if buildInfo.BuildVersion == nil || buildInfo.BuildVersion.Compare(minBuildVersion) < 0 {
+			if rebuildLogger != nil {
+				rebuildLogger.Info("index build version is before minBuildVersion, rebuilding the index", "indexBuildVersion", buildInfo.BuildVersion, "minBuildVersion", minBuildVersion)
+			}
+			return true
+		}
+	}
+
+	return false
+}
+
+type rebuildRequest struct {
+	NamespacedResource
+
+	minBuildTime    time.Time       // if not zero, only rebuild index if it has been built before this timestamp
+	minBuildVersion *semver.Version // if not nil, only rebuild index with build version older than this.
 }
 
 func (s *searchSupport) getOrCreateIndex(ctx context.Context, key NamespacedResource, reason string) (ResourceIndex, error) {
diff --git a/pkg/storage/unified/resource/search_test.go b/pkg/storage/unified/resource/search_test.go
index be34e3a5724..270719af2a7 100644
--- a/pkg/storage/unified/resource/search_test.go
+++ b/pkg/storage/unified/resource/search_test.go
@@ -9,11 +9,16 @@ import (
 	"testing"
 	"time"
 
+	"log/slog"
+
+	"github.com/Masterminds/semver"
 	"github.com/grafana/authlib/types"
 	"github.com/stretchr/testify/mock"
 	"github.com/stretchr/testify/require"
 	"go.opentelemetry.io/otel/trace/noop"
 
+	dashboardv1 "github.com/grafana/grafana/apps/dashboard/pkg/apis/dashboard/v1beta1"
+	"github.com/grafana/grafana/pkg/infra/log/logtest"
 	"github.com/grafana/grafana/pkg/storage/unified/resourcepb"
 )
 
@@ -27,6 +32,12 @@ type MockResourceIndex struct {
 
 	updateIndexMu    sync.Mutex
 	updateIndexCalls []string
+
+	buildInfo IndexBuildInfo
+}
+
+func (m *MockResourceIndex) BuildInfo() (IndexBuildInfo, error) {
+	return m.buildInfo, nil
 }
 
 func (m *MockResourceIndex) BulkIndex(req *BulkIndexRequest) error {
@@ -120,10 +131,11 @@ func (m *mockStorageBackend) ListModifiedSince(ctx context.Context, key Namespac
 
 // mockSearchBackend implements SearchBackend for testing with tracking capabilities
 type mockSearchBackend struct {
-	mu                   sync.Mutex
-	buildIndexCalls      []buildIndexCall
-	buildEmptyIndexCalls []buildEmptyIndexCall
-	cache                map[NamespacedResource]ResourceIndex
+	openIndexes []NamespacedResource
+
+	mu              sync.Mutex
+	buildIndexCalls []buildIndexCall
+	cache           map[NamespacedResource]ResourceIndex
 }
 
 type buildIndexCall struct {
@@ -132,12 +144,6 @@ type buildIndexCall struct {
 	fields SearchableDocumentFields
 }
 
-type buildEmptyIndexCall struct {
-	key    NamespacedResource
-	size   int64 // should be 0 for empty indexes
-	fields SearchableDocumentFields
-}
-
 func (m *mockSearchBackend) GetIndex(ctx context.Context, key NamespacedResource) (ResourceIndex, error) {
 	m.mu.Lock()
 	defer m.mu.Unlock()
@@ -165,21 +171,11 @@ func (m *mockSearchBackend) BuildIndex(ctx context.Context, key NamespacedResour
 
 	// Determine if this is an empty index based on size
 	// Empty indexes are characterized by size == 0
-	if size == 0 {
-		// This is an empty index (buildEmptyIndex was called)
-		m.buildEmptyIndexCalls = append(m.buildEmptyIndexCalls, buildEmptyIndexCall{
-			key:    key,
-			size:   size,
-			fields: fields,
-		})
-	} else {
-		// This is a normal index (build was called)
-		m.buildIndexCalls = append(m.buildIndexCalls, buildIndexCall{
-			key:    key,
-			size:   size,
-			fields: fields,
-		})
-	}
+	m.buildIndexCalls = append(m.buildIndexCalls, buildIndexCall{
+		key:    key,
+		size:   size,
+		fields: fields,
+	})
 
 	return index, nil
 }
@@ -188,6 +184,10 @@ func (m *mockSearchBackend) TotalDocs() int64 {
 	return 0
 }
 
+func (m *mockSearchBackend) GetOpenIndexes() []NamespacedResource {
+	return m.openIndexes
+}
+
 func TestSearchGetOrCreateIndex(t *testing.T) {
 	// Setup mock implementations
 	storage := &mockStorageBackend{
@@ -195,22 +195,17 @@ func TestSearchGetOrCreateIndex(t *testing.T) {
 			{NamespacedResource: NamespacedResource{Namespace: "ns", Group: "group", Resource: "resource"}, Count: 50, ResourceVersion: 11111111},
 		},
 	}
-	search := &mockSearchBackend{
-		buildIndexCalls:      []buildIndexCall{},
-		buildEmptyIndexCalls: []buildEmptyIndexCall{},
-	}
+	search := &mockSearchBackend{}
 	supplier := &TestDocumentBuilderSupplier{
 		GroupsResources: map[string]string{
 			"group": "resource",
 		},
 	}
 
-	// Create search support with the specified initMaxSize
 	opts := SearchOptions{
-		Backend:       search,
-		Resources:     supplier,
-		WorkerThreads: 1,
-		InitMinCount:  1, // set min count to default for this test
+		Backend:      search,
+		Resources:    supplier,
+		InitMinCount: 1, // set min count to default for this test
 	}
 
 	support, err := newSearchSupport(opts, storage, nil, nil, noop.NewTracerProvider().Tracer("test"), nil, nil)
@@ -250,9 +245,6 @@ func TestSearchGetOrCreateIndexWithIndexUpdate(t *testing.T) {
 	}
 	failedErr := fmt.Errorf("failed to update index")
 	search := &mockSearchBackend{
-		buildIndexCalls:      []buildIndexCall{},
-		buildEmptyIndexCalls: []buildEmptyIndexCall{},
-
 		cache: map[NamespacedResource]ResourceIndex{
 			{Namespace: "ns", Group: "group", Resource: "bad"}: &MockResourceIndex{
 				updateIndexError: failedErr,
@@ -265,12 +257,10 @@ func TestSearchGetOrCreateIndexWithIndexUpdate(t *testing.T) {
 		},
 	}
 
-	// Create search support with the specified initMaxSize
 	opts := SearchOptions{
-		Backend:       search,
-		Resources:     supplier,
-		WorkerThreads: 1,
-		InitMinCount:  1, // set min count to default for this test
+		Backend:      search,
+		Resources:    supplier,
+		InitMinCount: 1, // set min count to default for this test
 	}
 
 	// Enable searchAfterWrite
@@ -317,12 +307,10 @@ func TestSearchGetOrCreateIndexWithCancellation(t *testing.T) {
 		},
 	}
 
-	// Create search support with the specified initMaxSize
 	opts := SearchOptions{
-		Backend:       search,
-		Resources:     supplier,
-		WorkerThreads: 1,
-		InitMinCount:  1, // set min count to default for this test
+		Backend:      search,
+		Resources:    supplier,
+		InitMinCount: 1, // set min count to default for this test
 	}
 
 	support, err := newSearchSupport(opts, storage, nil, nil, noop.NewTracerProvider().Tracer("test"), nil, nil)
@@ -381,3 +369,350 @@ func (m *slowSearchBackendWithCache) BuildIndex(ctx context.Context, key Namespa
 	}
 	return idx, nil
 }
+
+func TestCombineBuildRequests(t *testing.T) {
+	type testcase struct {
+		a, b  rebuildRequest
+		exp   rebuildRequest
+		expOK bool
+	}
+
+	now := time.Now()
+	for name, tc := range map[string]testcase{
+		"mismatched resource": {
+			a:     rebuildRequest{NamespacedResource: NamespacedResource{Namespace: "a", Group: "a", Resource: "a"}},
+			b:     rebuildRequest{NamespacedResource: NamespacedResource{Namespace: "b", Group: "b", Resource: "b"}},
+			expOK: false,
+		},
+		"equal values": {
+			a:     rebuildRequest{minBuildTime: now, minBuildVersion: semver.MustParse("10.15.20")},
+			b:     rebuildRequest{minBuildTime: now, minBuildVersion: semver.MustParse("10.15.20")},
+			expOK: true,
+			exp:   rebuildRequest{minBuildTime: now, minBuildVersion: semver.MustParse("10.15.20")},
+		},
+		"empty field": {
+			a:     rebuildRequest{minBuildTime: now},
+			b:     rebuildRequest{minBuildVersion: semver.MustParse("10.15.20")},
+			expOK: true,
+			exp:   rebuildRequest{minBuildTime: now, minBuildVersion: semver.MustParse("10.15.20")},
+		},
+		"use max build time": {
+			a:     rebuildRequest{minBuildTime: now.Add(2 * time.Hour)},
+			b:     rebuildRequest{minBuildTime: now.Add(-time.Hour)},
+			expOK: true,
+			exp:   rebuildRequest{minBuildTime: now.Add(2 * time.Hour)},
+		},
+		"use max version": {
+			a:     rebuildRequest{minBuildVersion: semver.MustParse("12.10.99")},
+			b:     rebuildRequest{minBuildVersion: semver.MustParse("10.15.20")},
+			expOK: true,
+			exp:   rebuildRequest{minBuildVersion: semver.MustParse("12.10.99")},
+		},
+		"both fields": {
+			a:     rebuildRequest{minBuildTime: now.Add(2 * time.Hour), minBuildVersion: semver.MustParse("12.10.99")},
+			b:     rebuildRequest{minBuildTime: now.Add(-time.Hour), minBuildVersion: semver.MustParse("10.15.20")},
+			expOK: true,
+			exp:   rebuildRequest{minBuildTime: now.Add(2 * time.Hour), minBuildVersion: semver.MustParse("12.10.99")},
+		},
+	} {
+		t.Run(name, func(t *testing.T) {
+			res1, ok := combineRebuildRequests(tc.a, tc.b)
+			require.Equal(t, tc.expOK, ok)
+			if ok {
+				require.Equal(t, tc.exp, res1)
+			}
+
+			// commutativity
+			res2, ok := combineRebuildRequests(tc.b, tc.a)
+			require.Equal(t, tc.expOK, ok)
+			if ok {
+				require.Equal(t, tc.exp, res2)
+			}
+		})
+	}
+}
+
+func TestShouldRebuildIndex(t *testing.T) {
+	type testcase struct {
+		buildInfo       IndexBuildInfo
+		minTime         time.Time
+		minBuildVersion *semver.Version
+
+		expected bool
+	}
+
+	now := time.Now()
+
+	for name, tc := range map[string]testcase{
+		"empty build info, with no rebuild conditions": {
+			buildInfo: IndexBuildInfo{},
+			expected:  false,
+		},
+		"empty build info, with minTime": {
+			buildInfo: IndexBuildInfo{},
+			minTime:   now,
+			expected:  true,
+		},
+		"empty build info, with minVersion": {
+			buildInfo:       IndexBuildInfo{},
+			minBuildVersion: semver.MustParse("10.15.20"),
+			expected:        true,
+		},
+		"build time before min time": {
+			buildInfo: IndexBuildInfo{BuildTime: now.Add(-2 * time.Hour)},
+			minTime:   now,
+			expected:  true,
+		},
+		"build time after min time": {
+			buildInfo: IndexBuildInfo{BuildTime: now.Add(2 * time.Hour)},
+			minTime:   now,
+			expected:  false,
+		},
+		"build version before min version": {
+			buildInfo:       IndexBuildInfo{BuildVersion: semver.MustParse("10.15.19")},
+			minBuildVersion: semver.MustParse("10.15.20"),
+			expected:        true,
+		},
+		"build version after min version": {
+			buildInfo:       IndexBuildInfo{BuildVersion: semver.MustParse("11.0.0")},
+			minBuildVersion: semver.MustParse("10.15.20"),
+			expected:        false,
+		},
+	} {
+		t.Run(name, func(t *testing.T) {
+			res := shouldRebuildIndex(tc.minBuildVersion, tc.buildInfo, tc.minTime, slog.New(&logtest.NopHandler{}))
+			require.Equal(t, tc.expected, res)
+		})
+	}
+}
+
+func TestFindIndexesForRebuild(t *testing.T) {
+	storage := &mockStorageBackend{
+		resourceStats: []ResourceStats{
+			{NamespacedResource: NamespacedResource{Namespace: "ns", Group: "group", Resource: "resource"}, Count: 50, ResourceVersion: 11111111},
+		},
+	}
+
+	now := time.Now()
+
+	search := &mockSearchBackend{
+		openIndexes: []NamespacedResource{
+			{Namespace: "resource-2h-v5", Group: "group", Resource: "folder"},
+			{Namespace: "resource-2h-v6", Group: "group", Resource: "folder"},
+			{Namespace: "resource-10h-v5", Group: "group", Resource: "folder"},
+			{Namespace: "resource-10h-v6", Group: "group", Resource: "folder"},
+			{Namespace: "resource-v5", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE},
+			{Namespace: "resource-v6", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE},
+			{Namespace: "resource-2h-v5", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE},
+			{Namespace: "resource-2h-v6", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE},
+
+			// We report this index as open, but it's really not. This can happen if index expires between the call
+			// to GetOpenIndexes and the call to GetIndex.
+			{Namespace: "ns", Group: "group", Resource: "missing"},
+		},
+
+		cache: map[NamespacedResource]ResourceIndex{
+			// To be rebuilt because of minVersion
+			{Namespace: "resource-2h-v5", Group: "group", Resource: "folder"}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now.Add(-2 * time.Hour), BuildVersion: semver.MustParse("5.0.0")},
+			},
+
+			// Not rebuilt
+			{Namespace: "resource-2h-v6", Group: "group", Resource: "folder"}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now.Add(-2 * time.Hour), BuildVersion: semver.MustParse("6.0.0")},
+			},
+
+			// To be rebuilt because of minTime
+			{Namespace: "resource-10h-v5", Group: "group", Resource: "folder"}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now.Add(-10 * time.Hour), BuildVersion: semver.MustParse("5.0.0")},
+			},
+
+			// To be rebuilt because of minTime
+			{Namespace: "resource-10h-v6", Group: "group", Resource: "folder"}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now.Add(-10 * time.Hour), BuildVersion: semver.MustParse("6.0.0")},
+			},
+
+			// To be rebuilt because of minVersion
+			{Namespace: "resource-v5", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now, BuildVersion: semver.MustParse("5.0.0")},
+			},
+
+			// Not rebuilt
+			{Namespace: "resource-v6", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now, BuildVersion: semver.MustParse("6.0.0")},
+			},
+
+			// To be rebuilt because of minTime (1h for dashboards)
+			{Namespace: "resource-2h-v5", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now.Add(-2 * time.Hour), BuildVersion: semver.MustParse("5.0.0")},
+			},
+
+			// To be rebuilt because of minTime (1h for dashboards)
+			{Namespace: "resource-2h-v6", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now.Add(-2 * time.Hour), BuildVersion: semver.MustParse("6.0.0")},
+			},
+		},
+	}
+
+	supplier := &TestDocumentBuilderSupplier{
+		GroupsResources: map[string]string{
+			"group": "resource",
+		},
+	}
+
+	opts := SearchOptions{
+		Backend:   search,
+		Resources: supplier,
+
+		DashboardIndexMaxAge: 1 * time.Hour,
+		MaxIndexAge:          5 * time.Hour,
+		MinBuildVersion:      semver.MustParse("5.5.5"),
+	}
+
+	support, err := newSearchSupport(opts, storage, nil, nil, noop.NewTracerProvider().Tracer("test"), nil, nil)
+	require.NoError(t, err)
+	require.NotNil(t, support)
+
+	support.findIndexesToRebuild(context.Background(), now)
+	require.Equal(t, 6, support.rebuildQueue.Len())
+
+	now5m := now.Add(5 * time.Minute)
+
+	// Running findIndexesToRebuild again should not add any new indexes to the rebuild queue, and all existing
+	// ones should be "combined" with new ones (this will "bump" minBuildTime)
+	support.findIndexesToRebuild(context.Background(), now5m)
+	require.Equal(t, 6, support.rebuildQueue.Len())
+
+	// Values that we expect to find in rebuild requests.
+	minBuildVersion := semver.MustParse("5.5.5")
+	minBuildTime := now5m.Add(-5 * time.Hour)
+	minBuildTimeDashboard := now5m.Add(-1 * time.Hour)
+
+	vals := support.rebuildQueue.Elements()
+	require.ElementsMatch(t, vals, []rebuildRequest{
+		{NamespacedResource: NamespacedResource{Namespace: "resource-2h-v5", Group: "group", Resource: "folder"}, minBuildVersion: minBuildVersion, minBuildTime: minBuildTime},
+		{NamespacedResource: NamespacedResource{Namespace: "resource-10h-v5", Group: "group", Resource: "folder"}, minBuildVersion: minBuildVersion, minBuildTime: minBuildTime},
+		{NamespacedResource: NamespacedResource{Namespace: "resource-10h-v6", Group: "group", Resource: "folder"}, minBuildVersion: minBuildVersion, minBuildTime: minBuildTime},
+
+		{NamespacedResource: NamespacedResource{Namespace: "resource-v5", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}, minBuildVersion: minBuildVersion, minBuildTime: minBuildTimeDashboard},
+		{NamespacedResource: NamespacedResource{Namespace: "resource-2h-v5", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}, minBuildVersion: minBuildVersion, minBuildTime: minBuildTimeDashboard},
+		{NamespacedResource: NamespacedResource{Namespace: "resource-2h-v6", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}, minBuildVersion: minBuildVersion, minBuildTime: minBuildTimeDashboard},
+	})
+}
+
+func TestRebuildIndexes(t *testing.T) {
+	storage := &mockStorageBackend{}
+
+	now := time.Now()
+
+	search := &mockSearchBackend{
+		cache: map[NamespacedResource]ResourceIndex{
+			{Namespace: "idx1", Group: "group", Resource: "res"}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildVersion: semver.MustParse("5.0.0")},
+			},
+
+			{Namespace: "idx2", Group: "group", Resource: "res"}: &MockResourceIndex{
+				buildInfo: IndexBuildInfo{BuildTime: now.Add(-2 * time.Hour)},
+			},
+
+			{Namespace: "idx3", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}: &MockResourceIndex{},
+		},
+	}
+
+	supplier := &TestDocumentBuilderSupplier{
+		GroupsResources: map[string]string{
+			"group": "resource",
+		},
+	}
+
+	opts := SearchOptions{
+		Backend:   search,
+		Resources: supplier,
+	}
+
+	support, err := newSearchSupport(opts, storage, nil, nil, noop.NewTracerProvider().Tracer("test"), nil, nil)
+	require.NoError(t, err)
+	require.NotNil(t, support)
+
+	// Note: we can only rebuild each index once, after that it "loses" it's build info.
+
+	t.Run("Don't rebuild if min build version is old", func(t *testing.T) {
+		checkRebuildIndex(t, support, rebuildRequest{
+			NamespacedResource: NamespacedResource{Namespace: "idx1", Group: "group", Resource: "res"},
+			minBuildVersion:    semver.MustParse("4.5"),
+		}, true, false)
+	})
+
+	t.Run("Rebuild if min build version is more recent", func(t *testing.T) {
+		checkRebuildIndex(t, support, rebuildRequest{
+			NamespacedResource: NamespacedResource{Namespace: "idx1", Group: "group", Resource: "res"},
+			minBuildVersion:    semver.MustParse("5.5.5"),
+		}, true, true)
+	})
+
+	t.Run("Don't rebuild if min build time is very old", func(t *testing.T) {
+		checkRebuildIndex(t, support, rebuildRequest{
+			NamespacedResource: NamespacedResource{Namespace: "idx2", Group: "group", Resource: "res"},
+			minBuildTime:       now.Add(-5 * time.Hour),
+		}, true, false)
+	})
+
+	t.Run("Rebuild if min build time is more recent", func(t *testing.T) {
+		checkRebuildIndex(t, support, rebuildRequest{
+			NamespacedResource: NamespacedResource{Namespace: "idx2", Group: "group", Resource: "res"},
+			minBuildTime:       now.Add(-1 * time.Hour),
+		}, true, true)
+	})
+
+	t.Run("Don't rebuild if index doesn't exist.", func(t *testing.T) {
+		checkRebuildIndex(t, support, rebuildRequest{
+			NamespacedResource: NamespacedResource{Namespace: "unknown", Group: "group", Resource: "res"},
+			minBuildTime:       now.Add(-5 * time.Hour),
+		}, false, true)
+	})
+
+	t.Run("Rebuild dashboard index (it has no build info), verify that builders cache was emptied.", func(t *testing.T) {
+		dashKey := NamespacedResource{Namespace: "idx3", Group: "group", Resource: dashboardv1.DASHBOARD_RESOURCE}
+
+		support.builders.ns.Add(dashKey, &MockDocumentBuilder{})
+		_, ok := support.builders.ns.Get(dashKey)
+		require.True(t, ok)
+
+		checkRebuildIndex(t, support, rebuildRequest{
+			NamespacedResource: dashKey,
+			minBuildTime:       now,
+		}, true, true)
+
+		// Verify that builders cache was emptied.
+		_, ok = support.builders.ns.Get(dashKey)
+		require.False(t, ok)
+	})
+}
+
+func checkRebuildIndex(t *testing.T, support *searchSupport, req rebuildRequest, indexExists, expectedRebuild bool) {
+	ctx := context.Background()
+
+	idxBefore, err := support.search.GetIndex(ctx, req.NamespacedResource)
+	require.NoError(t, err)
+	if indexExists {
+		require.NotNil(t, idxBefore, "index should exist before rebuildIndex")
+	} else {
+		require.Nil(t, idxBefore, "index should not exist before rebuildIndex")
+	}
+
+	support.rebuildIndex(ctx, req)
+
+	idxAfter, err := support.search.GetIndex(ctx, req.NamespacedResource)
+	require.NoError(t, err)
+
+	if indexExists {
+		require.NotNil(t, idxAfter, "index should exist after rebuildIndex")
+		if expectedRebuild {
+			require.NotSame(t, idxBefore, idxAfter, "index should be rebuilt")
+		} else {
+			require.Same(t, idxBefore, idxAfter, "index should not be rebuilt")
+		}
+	} else {
+		require.Nil(t, idxAfter, "index should not exist after rebuildIndex")
+	}
+}
diff --git a/pkg/storage/unified/resource/server.go b/pkg/storage/unified/resource/server.go
index 575d1dd608b..f2613d6a3cf 100644
--- a/pkg/storage/unified/resource/server.go
+++ b/pkg/storage/unified/resource/server.go
@@ -11,6 +11,7 @@ import (
 	"sync/atomic"
 	"time"
 
+	"github.com/Masterminds/semver"
 	"github.com/google/uuid"
 	"github.com/prometheus/client_golang/prometheus"
 	"go.opentelemetry.io/otel/trace"
@@ -21,7 +22,6 @@ import (
 
 	claims "github.com/grafana/authlib/types"
 	"github.com/grafana/dskit/backoff"
-	"github.com/grafana/dskit/ring"
 
 	"github.com/grafana/grafana/pkg/apimachinery/utils"
 	"github.com/grafana/grafana/pkg/apimachinery/validation"
@@ -179,15 +179,22 @@ type SearchOptions struct {
 	Resources DocumentBuilderSupplier
 
 	// How many threads should build indexes
-	WorkerThreads int
+	InitWorkerThreads int
 
 	// Skip building index on startup for small indexes
 	InitMinCount int
 
-	// Interval for periodic index rebuilds (0 disables periodic rebuilds)
-	RebuildInterval time.Duration
+	// How often to rebuild dashboard index. 0 disables periodic rebuilds.
+	DashboardIndexMaxAge time.Duration
 
-	Ring *ring.Ring
+	// Maximum age of file-based index that can be reused. Ignored if zero.
+	MaxIndexAge time.Duration
+
+	// Minimum build version for reusing file-based indexes. Ignored if nil.
+	MinBuildVersion *semver.Version
+
+	// Number of workers to use for index rebuilds.
+	IndexRebuildWorkers int
 }
 
 type ResourceServerOptions struct {
@@ -422,6 +429,10 @@ func (s *server) Stop(ctx context.Context) error {
 		}
 	}
 
+	if s.search != nil {
+		s.search.stop()
+	}
+
 	// Stops the streaming
 	s.cancel()
 
diff --git a/pkg/storage/unified/search/bleve.go b/pkg/storage/unified/search/bleve.go
index ef06f585363..7e96a10da26 100644
--- a/pkg/storage/unified/search/bleve.go
+++ b/pkg/storage/unified/search/bleve.go
@@ -52,7 +52,7 @@ const (
 // Keys used to store internal data in index.
 const (
 	internalRVKey        = "rv"         // Encoded as big-endian int64
-	internalBuildInfoKey = "build_info" // Encoded as JSON of IndexBuildInfo struct
+	internalBuildInfoKey = "build_info" // Encoded as JSON of buildInfo struct
 )
 
 var _ resource.SearchBackend = &bleveBackend{}
@@ -75,9 +75,6 @@ type BleveOptions struct {
 
 	BuildVersion string
 
-	MaxFileIndexAge time.Duration   // Maximum age of file-based index that can be reused. Ignored if zero.
-	MinBuildVersion *semver.Version // Minimum build version for reusing file-based indexes. Ignored if nil.
-
 	Logger *slog.Logger
 
 	UseFullNgram bool
@@ -179,6 +176,17 @@ func (b *bleveBackend) GetIndex(_ context.Context, key resource.NamespacedResour
 	return idx, nil
 }
 
+func (b *bleveBackend) GetOpenIndexes() []resource.NamespacedResource {
+	b.cacheMx.RLock()
+	defer b.cacheMx.RUnlock()
+
+	result := make([]resource.NamespacedResource, 0, len(b.cache))
+	for key := range b.cache {
+		result = append(result, key)
+	}
+	return result
+}
+
 func (b *bleveBackend) getCachedIndex(key resource.NamespacedResource, now time.Time) *bleveIndex {
 	// Check index with read-lock first.
 	b.cacheMx.RLock()
@@ -318,7 +326,7 @@ func newBleveIndex(path string, mapper mapping.IndexMapping, buildTime time.Time
 		return nil, err
 	}
 
-	bi := IndexBuildInfo{
+	bi := buildInfo{
 		BuildTime:    buildTime.Unix(),
 		BuildVersion: buildVersion,
 	}
@@ -336,29 +344,11 @@ func newBleveIndex(path string, mapper mapping.IndexMapping, buildTime time.Time
 	return ix, nil
 }
 
-type IndexBuildInfo struct {
+type buildInfo struct {
 	BuildTime    int64  `json:"build_time"`    // Unix seconds timestamp of time when the index was built
 	BuildVersion string `json:"build_version"` // Grafana version used when building the index
 }
 
-func (bi IndexBuildInfo) GetBuildTime() time.Time {
-	if bi.BuildTime == 0 {
-		return time.Time{}
-	}
-	return time.Unix(bi.BuildTime, 0)
-}
-
-func (bi IndexBuildInfo) GetBuildVersion() *semver.Version {
-	if bi.BuildVersion == "" {
-		return nil
-	}
-	v, err := semver.NewVersion(bi.BuildVersion)
-	if err != nil {
-		return nil
-	}
-	return v
-}
-
 // BuildIndex builds an index from scratch or retrieves it from the filesystem.
 // If built successfully, the new index replaces the old index in the cache (if there was any).
 // Existing index in the file system is reused, if it exists, and if size indicates that we should use file-based index, and rebuild is not true.
@@ -435,11 +425,7 @@ func (b *bleveBackend) BuildIndex(
 		// This happens on startup, or when memory-based index has expired. (We don't expire file-based indexes)
 		// If we do have an unexpired cached index already, we always build a new index from scratch.
 		if cachedIndex == nil && !rebuild {
-			minBuildTime := time.Time{}
-			if b.opts.MaxFileIndexAge > 0 {
-				minBuildTime = time.Now().Add(-b.opts.MaxFileIndexAge)
-			}
-			index, fileIndexName, indexRV = b.findPreviousFileBasedIndex(resourceDir, minBuildTime, b.opts.MinBuildVersion)
+			index, fileIndexName, indexRV = b.findPreviousFileBasedIndex(resourceDir)
 		}
 
 		if index != nil {
@@ -621,18 +607,6 @@ func isPathWithinRoot(path, absoluteRoot string) bool {
 	return true
 }
 
-// cacheKeys returns list of keys for indexes in the cache (including possibly expired ones).
-func (b *bleveBackend) cacheKeys() []resource.NamespacedResource {
-	b.cacheMx.RLock()
-	defer b.cacheMx.RUnlock()
-
-	keys := make([]resource.NamespacedResource, 0, len(b.cache))
-	for k := range b.cache {
-		keys = append(keys, k)
-	}
-	return keys
-}
-
 // TotalDocs returns the total number of documents across all indices
 func (b *bleveBackend) TotalDocs() int64 {
 	var totalDocs int64
@@ -640,7 +614,7 @@ func (b *bleveBackend) TotalDocs() int64 {
 	// We do this to avoid keeping a lock for the entire TotalDocs function, since DocCount may be slow (due to disk access).
 
 	now := time.Now()
-	for _, key := range b.cacheKeys() {
+	for _, key := range b.GetOpenIndexes() {
 		idx := b.getCachedIndex(key, now)
 		if idx == nil {
 			continue
@@ -658,7 +632,7 @@ func formatIndexName(now time.Time) string {
 	return now.Format("20060102-150405")
 }
 
-func (b *bleveBackend) findPreviousFileBasedIndex(resourceDir string, minBuildTime time.Time, minBuildVersion *semver.Version) (bleve.Index, string, int64) {
+func (b *bleveBackend) findPreviousFileBasedIndex(resourceDir string) (bleve.Index, string, int64) {
 	entries, err := os.ReadDir(resourceDir)
 	if err != nil {
 		return nil, "", 0
@@ -684,31 +658,6 @@ func (b *bleveBackend) findPreviousFileBasedIndex(resourceDir string, minBuildTi
 			continue
 		}
 
-		buildInfo, err := getBuildInfo(idx)
-		if err != nil {
-			b.log.Error("error getting build info from index", "indexDir", indexDir, "err", err)
-			_ = idx.Close()
-			continue
-		}
-
-		if !minBuildTime.IsZero() {
-			bt := buildInfo.GetBuildTime()
-			if bt.IsZero() || bt.Before(minBuildTime) {
-				b.log.Debug("index build time is before minBuildTime, not reusing the index", "indexDir", indexDir, "indexBuildTime", bt, "minBuildTime", minBuildTime)
-				_ = idx.Close()
-				continue
-			}
-		}
-
-		if minBuildVersion != nil {
-			bv := buildInfo.GetBuildVersion()
-			if bv == nil || bv.Compare(minBuildVersion) < 0 {
-				b.log.Debug("index build version is before minBuildVersion, not reusing the index", "indexDir", indexDir, "indexBuildVersion", bv, "minBuildVersion", minBuildVersion)
-				_ = idx.Close()
-				continue
-			}
-		}
-
 		return idx, indexName, indexRV
 	}
 
@@ -878,21 +827,46 @@ func getRV(index bleve.Index) (int64, error) {
 	return int64(binary.BigEndian.Uint64(raw)), nil
 }
 
-func getBuildInfo(index bleve.Index) (IndexBuildInfo, error) {
+func getBuildInfo(index bleve.Index) (buildInfo, error) {
 	raw, err := index.GetInternal([]byte(internalBuildInfoKey))
 	if err != nil {
-		return IndexBuildInfo{}, err
+		return buildInfo{}, err
 	}
 
 	if len(raw) == 0 {
-		return IndexBuildInfo{}, nil
+		return buildInfo{}, nil
 	}
 
-	res := IndexBuildInfo{}
+	res := buildInfo{}
 	err = json.Unmarshal(raw, &res)
 	return res, err
 }
 
+func (b *bleveIndex) BuildInfo() (resource.IndexBuildInfo, error) {
+	bi, err := getBuildInfo(b.index)
+	if err != nil {
+		return resource.IndexBuildInfo{}, err
+	}
+
+	bt := time.Time{}
+	if bi.BuildTime > 0 {
+		bt = time.Unix(bi.BuildTime, 0)
+	}
+
+	var bv *semver.Version
+	if bi.BuildVersion != "" {
+		v, err := semver.NewVersion(bi.BuildVersion)
+		if err == nil {
+			bv = v
+		}
+	}
+
+	return resource.IndexBuildInfo{
+		BuildTime:    bt,
+		BuildVersion: bv,
+	}, nil
+}
+
 func (b *bleveIndex) ListManagedObjects(ctx context.Context, req *resourcepb.ListManagedObjectsRequest) (*resourcepb.ListManagedObjectsResponse, error) {
 	if req.NextPageToken != "" {
 		return nil, fmt.Errorf("next page not implemented yet")
diff --git a/pkg/storage/unified/search/bleve_test.go b/pkg/storage/unified/search/bleve_test.go
index 347195786a5..62725adda5d 100644
--- a/pkg/storage/unified/search/bleve_test.go
+++ b/pkg/storage/unified/search/bleve_test.go
@@ -14,7 +14,6 @@ import (
 	"testing"
 	"time"
 
-	"github.com/Masterminds/semver"
 	"github.com/blevesearch/bleve/v2"
 	authlib "github.com/grafana/authlib/types"
 	"github.com/prometheus/client_golang/prometheus"
@@ -827,24 +826,6 @@ func withRootDir(root string) setupOption {
 	}
 }
 
-func withBuildVersion(version string) setupOption {
-	return func(options *BleveOptions) {
-		options.BuildVersion = version
-	}
-}
-
-func withMinBuildVersion(version *semver.Version) setupOption {
-	return func(options *BleveOptions) {
-		options.MinBuildVersion = version
-	}
-}
-
-func withMaxFileIndexAge(maxAge time.Duration) setupOption {
-	return func(options *BleveOptions) {
-		options.MaxFileIndexAge = maxAge
-	}
-}
-
 func withOwnsIndexFn(fn func(key resource.NamespacedResource) (bool, error)) setupOption {
 	return func(options *BleveOptions) {
 		options.OwnsIndex = fn
@@ -978,81 +959,39 @@ func TestBuildIndex(t *testing.T) {
 		Resource:  "resource",
 	}
 
-	const alwaysRebuildDueToAge = 1 * time.Nanosecond
-	const neverRebuildDueToAge = 1 * time.Hour
-
 	for _, rebuild := range []bool{false, true} {
-		for _, version := range []string{"", "12.5.123"} {
-			for _, minBuildVersion := range []*semver.Version{nil, semver.MustParse("12.0.0"), semver.MustParse("13.0.0")} {
-				for _, maxIndexAge := range []time.Duration{0, alwaysRebuildDueToAge, neverRebuildDueToAge} {
-					shouldRebuild := rebuild
-					if minBuildVersion != nil {
-						shouldRebuild = shouldRebuild || version == "" || minBuildVersion.GreaterThan(semver.MustParse(version))
-					}
-					if maxIndexAge > 0 {
-						shouldRebuild = shouldRebuild || maxIndexAge == alwaysRebuildDueToAge
-					}
+		testName := fmt.Sprintf("rebuild=%t", rebuild)
 
-					testName := ""
-					if shouldRebuild {
-						testName += "should REBUILD index"
-					} else {
-						testName += "should REUSE index"
-					}
+		t.Run(testName, func(t *testing.T) {
+			tmpDir := t.TempDir()
 
-					if rebuild {
-						testName += " when rebuild is true"
-					} else {
-						testName += " when rebuild is false"
-					}
+			const (
+				firstIndexDocsCount  = 10
+				secondIndexDocsCount = 1000
+			)
 
-					if version != "" {
-						testName += " build version is " + version
-					} else {
-						testName += " build version is empty"
-					}
-
-					if minBuildVersion != nil {
-						testName += " min build version is " + minBuildVersion.String()
-					} else {
-						testName += " min build version is nil"
-					}
-
-					testName += " max index age is " + maxIndexAge.String()
-
-					t.Run(testName, func(t *testing.T) {
-						tmpDir := t.TempDir()
-
-						const (
-							firstIndexDocsCount  = 10
-							secondIndexDocsCount = 1000
-						)
-
-						{
-							backend, _ := setupBleveBackend(t, withFileThreshold(5), withRootDir(tmpDir), withBuildVersion(version))
-							_, err := backend.BuildIndex(context.Background(), ns, firstIndexDocsCount, nil, "test", indexTestDocs(ns, firstIndexDocsCount, 100), nil, rebuild)
-							require.NoError(t, err)
-							backend.Stop()
-						}
-
-						// Make sure we pass at least 1 nanosecond (alwaysRebuildDueToAge) to ensure that the index needs to be rebuild.
-						time.Sleep(1 * time.Millisecond)
-
-						newBackend, _ := setupBleveBackend(t, withFileThreshold(5), withRootDir(tmpDir), withBuildVersion(version), withMinBuildVersion(minBuildVersion), withMaxFileIndexAge(maxIndexAge))
-						idx, err := newBackend.BuildIndex(context.Background(), ns, secondIndexDocsCount, nil, "test", indexTestDocs(ns, secondIndexDocsCount, 100), nil, rebuild)
-						require.NoError(t, err)
-
-						cnt, err := idx.DocCount(context.Background(), "")
-						require.NoError(t, err)
-						if shouldRebuild {
-							require.Equal(t, int64(secondIndexDocsCount), cnt, "Index has been not rebuilt")
-						} else {
-							require.Equal(t, int64(firstIndexDocsCount), cnt, "Index has not been reused")
-						}
-					})
-				}
+			{
+				backend, _ := setupBleveBackend(t, withFileThreshold(5), withRootDir(tmpDir))
+				_, err := backend.BuildIndex(context.Background(), ns, firstIndexDocsCount, nil, "test", indexTestDocs(ns, firstIndexDocsCount, 100), nil, rebuild)
+				require.NoError(t, err)
+				backend.Stop()
 			}
-		}
+
+			// Make sure we pass at least 1 nanosecond (alwaysRebuildDueToAge) to ensure that the index needs to be rebuild.
+			time.Sleep(1 * time.Millisecond)
+
+			newBackend, _ := setupBleveBackend(t, withFileThreshold(5), withRootDir(tmpDir))
+			idx, err := newBackend.BuildIndex(context.Background(), ns, secondIndexDocsCount, nil, "test", indexTestDocs(ns, secondIndexDocsCount, 100), nil, rebuild)
+			require.NoError(t, err)
+
+			cnt, err := idx.DocCount(context.Background(), "")
+			require.NoError(t, err)
+			if rebuild {
+				require.Equal(t, int64(secondIndexDocsCount), cnt, "Index has been not rebuilt")
+			} else {
+				require.Equal(t, int64(firstIndexDocsCount), cnt, "Index has not been reused")
+			}
+		})
 	}
 }
 
diff --git a/pkg/storage/unified/search/options.go b/pkg/storage/unified/search/options.go
index a5bb1d52a8c..a719bebf32c 100644
--- a/pkg/storage/unified/search/options.go
+++ b/pkg/storage/unified/search/options.go
@@ -41,15 +41,13 @@ func NewSearchOptions(
 		}
 
 		bleve, err := NewBleveBackend(BleveOptions{
-			Root:            root,
-			FileThreshold:   int64(cfg.IndexFileThreshold), // fewer than X items will use a memory index
-			BatchSize:       cfg.IndexMaxBatchSize,         // This is the batch size for how many objects to add to the index at once
-			IndexCacheTTL:   cfg.IndexCacheTTL,             // How long to keep the index cache in memory
-			BuildVersion:    cfg.BuildVersion,
-			MaxFileIndexAge: cfg.MaxFileIndexAge,
-			MinBuildVersion: minVersion,
-			UseFullNgram:    features.IsEnabledGlobally(featuremgmt.FlagUnifiedStorageUseFullNgram),
-			OwnsIndex:       ownsIndexFn,
+			Root:          root,
+			FileThreshold: int64(cfg.IndexFileThreshold), // fewer than X items will use a memory index
+			BatchSize:     cfg.IndexMaxBatchSize,         // This is the batch size for how many objects to add to the index at once
+			IndexCacheTTL: cfg.IndexCacheTTL,             // How long to keep the index cache in memory
+			BuildVersion:  cfg.BuildVersion,
+			UseFullNgram:  features.IsEnabledGlobally(featuremgmt.FlagUnifiedStorageUseFullNgram),
+			OwnsIndex:     ownsIndexFn,
 		}, tracer, indexMetrics)
 
 		if err != nil {
@@ -57,11 +55,14 @@ func NewSearchOptions(
 		}
 
 		return resource.SearchOptions{
-			Backend:         bleve,
-			Resources:       docs,
-			WorkerThreads:   cfg.IndexWorkers,
-			InitMinCount:    cfg.IndexMinCount,
-			RebuildInterval: cfg.IndexRebuildInterval,
+			Backend:              bleve,
+			Resources:            docs,
+			InitWorkerThreads:    cfg.IndexWorkers,
+			IndexRebuildWorkers:  cfg.IndexRebuildWorkers,
+			InitMinCount:         cfg.IndexMinCount,
+			DashboardIndexMaxAge: cfg.IndexRebuildInterval,
+			MaxIndexAge:          cfg.MaxFileIndexAge,
+			MinBuildVersion:      minVersion,
 		}, nil
 	}
 	return resource.SearchOptions{}, nil
diff --git a/pkg/util/debouncer/queue.go b/pkg/util/debouncer/queue.go
new file mode 100644
index 00000000000..a6dd404da3a
--- /dev/null
+++ b/pkg/util/debouncer/queue.go
@@ -0,0 +1,119 @@
+package debouncer
+
+import (
+	"context"
+	"errors"
+	"slices"
+	"sync"
+)
+
+type CombineFn[T any] func(a, b T) (c T, ok bool)
+
+// Queue is a queue of elements. Elements added to the queue can be combined together by the provided combiner function.
+// Once the queue is closed, no more elements can be added, but Next() will still return remaining elements.
+type Queue[T any] struct {
+	combineFn CombineFn[T]
+
+	mu       sync.Mutex
+	elements []T
+	closed   bool
+	waitChan chan struct{} // if not nil, will be closed when new element is added
+}
+
+func NewQueue[T any](combineFn CombineFn[T]) *Queue[T] {
+	return &Queue[T]{
+		combineFn: combineFn,
+	}
+}
+
+func (q *Queue[T]) Len() int {
+	q.mu.Lock()
+	defer q.mu.Unlock()
+	return len(q.elements)
+}
+
+// Elements returns copy of the queue.
+func (q *Queue[T]) Elements() []T {
+	q.mu.Lock()
+	defer q.mu.Unlock()
+	return slices.Clone(q.elements)
+}
+
+func (q *Queue[T]) Add(n T) {
+	q.mu.Lock()
+	defer q.mu.Unlock()
+	if q.closed {
+		panic("queue already closed")
+	}
+
+	for i, e := range q.elements {
+		if c, ok := q.combineFn(e, n); ok {
+			// No need to signal, since we are not adding new element.
+			q.elements[i] = c
+			return
+		}
+	}
+
+	q.elements = append(q.elements, n)
+	q.notifyWaiters()
+}
+
+// Must be called with lock held.
+func (q *Queue[T]) notifyWaiters() {
+	if q.waitChan != nil {
+		// Wakes up all waiting goroutines (but also possibly zero, if they stopped waiting already).
+		close(q.waitChan)
+		q.waitChan = nil
+	}
+}
+
+var ErrClosed = errors.New("queue closed")
+
+// Next returns the next element in the queue. If no element is available, Next will block until
+// an element is added to the queue, or provided context is done.
+// If the queue is closed, ErrClosed is returned.
+func (q *Queue[T]) Next(ctx context.Context) (T, error) {
+	var zero T
+
+	q.mu.Lock()
+	unlockInDefer := true
+	defer func() {
+		if unlockInDefer {
+			q.mu.Unlock()
+		}
+	}()
+
+	for len(q.elements) == 0 {
+		if q.closed {
+			return zero, ErrClosed
+		}
+
+		// Wait for an element. Make sure there's a wait channel that we can use.
+		wch := q.waitChan
+		if wch == nil {
+			wch = make(chan struct{})
+			q.waitChan = wch
+		}
+		// Unlock before waiting
+		q.mu.Unlock()
+
+		select {
+		case <-ctx.Done():
+			unlockInDefer = false
+			return zero, ctx.Err()
+		case <-wch:
+			q.mu.Lock()
+		}
+	}
+
+	first := q.elements[0]
+	q.elements = q.elements[1:]
+	return first, nil
+}
+
+func (q *Queue[T]) Close() {
+	q.mu.Lock()
+	defer q.mu.Unlock()
+	q.closed = true
+	q.notifyWaiters()
+}
diff --git a/pkg/util/debouncer/queue_test.go b/pkg/util/debouncer/queue_test.go
new file mode 100644
index 00000000000..76106f8f99a
--- /dev/null
+++ b/pkg/util/debouncer/queue_test.go
@@ -0,0 +1,155 @@
+package debouncer
+
+import (
+	"context"
+	"errors"
+	"math/rand"
+	"sync"
+	"testing"
+	"time"
+
+	"github.com/stretchr/testify/require"
+	"go.uber.org/atomic"
+	"go.uber.org/goleak"
+)
+
+// This verifies that all goroutines spawned from tests are finished at the end of tests.
+// Applies to all tests in the package.
+func TestMain(m *testing.M) {
+	goleak.VerifyTestMain(m)
+}
+
+func TestQueueBasic(t *testing.T) {
+	q := NewQueue(func(a, b int) (c int, ok bool) {
+		return a + b, true
+	})
+
+	ctx, cancel := context.WithTimeout(context.Background(), 1*time.Millisecond)
+	defer cancel()
+	// Empty queue will time out.
+	require.Equal(t, context.DeadlineExceeded, nextErr(t, q, ctx))
+
+	q.Add(10)
+	require.Equal(t, 10, next(t, q))
+	require.Equal(t, 0, q.Len())
+
+	q.Add(20)
+	require.Equal(t, 20, next(t, q))
+	require.Equal(t, 0, q.Len())
+
+	q.Add(10)
+	require.Equal(t, 1, q.Len())
+	q.Add(20)
+	require.Equal(t, 1, q.Len())
+	require.Equal(t, 30, next(t, q))
+	require.Equal(t, 0, q.Len())
+
+	q.Add(100)
+	require.Equal(t, 1, q.Len())
+	q.Close()
+	require.Equal(t, 1, q.Len())
+	require.Equal(t, 100, next(t, q))
+	require.Equal(t, ErrClosed, nextErr(t, q, context.Background()))
+	require.Equal(t, 0, q.Len())
+
+	// We can call Next repeatedly, but will always get error.
+	require.Equal(t, ErrClosed, nextErr(t, q, context.Background()))
+}
+
+func TestQueueConcurrency(t *testing.T) {
+	q := NewQueue(func(a, b int64) (c int64, ok bool) {
+		// Combine the same numbers together.
+		if a == b {
+			return a + b, true
+		}
+		return 0, false
+	})
+
+	const numbers = 10000
+	const writeConcurrency = 50
+	const readConcurrency = 25
+
+	r := rand.New(rand.NewSource(time.Now().UnixNano()))
+
+	totalWrittenSum := atomic.NewInt64(0)
+	totalReadSum := atomic.NewInt64(0)
+	addCalls := atomic.NewInt64(0)
+	nextCalls := atomic.NewInt64(0)
+
+	// We will add some numbers to the queue.
+	writesWG := sync.WaitGroup{}
+	for i := 0; i < writeConcurrency; i++ {
+		writesWG.Add(1)
+		go func() {
+			defer writesWG.Done()
+			for j := 0; j < numbers; j++ {
+				v := r.Int63n(100) // Generate small number, so that we have a chance for combining some numbers.
+				q.Add(v)
+				addCalls.Inc()
+				totalWrittenSum.Add(v)
+			}
+		}()
+	}
+
+	readsWG := sync.WaitGroup{}
+	for i := 0; i < readConcurrency; i++ {
+		readsWG.Add(1)
+		go func() {
+			defer readsWG.Done()
+
+			for {
+				v, err := q.Next(context.Background())
+				if errors.Is(err, ErrClosed) {
+					return
+				}
+				require.NoError(t, err)
+
+				nextCalls.Inc()
+				totalReadSum.Add(v)
+			}
+		}()
+	}
+
+	writesWG.Wait()
+	// Close queue after sending all numbers. This signals readers that they can stop.
+	q.Close()
+
+	// Wait until all readers finish too.
+	readsWG.Wait()
+
+	// Verify that all numbers were sent, combined and received.
+	require.Equal(t, int64(writeConcurrency*numbers), addCalls.Load())
+	require.Equal(t, totalWrittenSum.Load(), totalReadSum.Load())
+	require.LessOrEqual(t, nextCalls.Load(), addCalls.Load())
+	t.Log("add calls:", addCalls.Load(), "next calls:", nextCalls.Load(), "total written sum:", totalWrittenSum.Load(), "total read sum:", totalReadSum.Load())
+}
+
+func TestQueueCloseUnblocksReaders(t *testing.T) {
+	q := NewQueue(func(a, b int) (c int, ok bool) {
+		return a + b, true
+	})
+
+	wg := sync.WaitGroup{}
+	wg.Add(1)
+	go func() {
+		defer wg.Done()
+		time.Sleep(50 * time.Millisecond)
+		q.Close()
+	}()
+
+	_, err := q.Next(context.Background())
+	require.ErrorIs(t, err, ErrClosed)
+
+	wg.Wait()
+}
+
+func next[T any](t *testing.T, q *Queue[T]) T {
+	v, err := q.Next(context.Background())
+	require.NoError(t, err)
+	return v
+}
+func nextErr[T any](t *testing.T, q *Queue[T], ctx context.Context) error {
+	_, err := q.Next(ctx)
+	require.Error(t, err)
+	return err
+}