diff --git a/src/flask/app.py b/src/flask/app.py
index 236a47a8..22dd3953 100644
--- a/src/flask/app.py
+++ b/src/flask/app.py
@@ -916,8 +916,8 @@ class Flask(Scaffold):
         if os.environ.get("FLASK_RUN_FROM_CLI") == "true":
             if not is_running_from_reloader():
                 click.secho(
-                    " * Ignoring a call to 'app.run()', the server is"
-                    " already being run with the 'flask run' command.\n"
+                    " * Ignoring a call to 'app.run()' that would block"
+                    " the current 'flask' CLI command.\n"
                     "   Only call 'app.run()' in an 'if __name__ =="
                     ' "__main__"\' guard.',
                     fg="red",
diff --git a/src/flask/cli.py b/src/flask/cli.py
index 321794b6..af29b2c1 100644
--- a/src/flask/cli.py
+++ b/src/flask/cli.py
@@ -715,6 +715,11 @@ class FlaskGroup(AppGroup):
         parent: click.Context | None = None,
         **extra: t.Any,
     ) -> click.Context:
+        # Set a flag to tell app.run to become a no-op. If app.run was
+        # not in a __name__ == __main__ guard, it would start the server
+        # when importing, blocking whatever command is being called.
+        os.environ["FLASK_RUN_FROM_CLI"] = "true"
+
         # Attempt to load .env and .flask env files. The --env-file
         # option can cause another file to be loaded.
         if get_load_dotenv(self.load_dotenv):
diff --git a/tests/test_cli.py b/tests/test_cli.py
index 7d83d865..fdd2212b 100644
--- a/tests/test_cli.py
+++ b/tests/test_cli.py
@@ -13,7 +13,6 @@ import pytest
 from _pytest.monkeypatch import notset
 from click.testing import CliRunner
 
-from flask import _app_ctx_stack
 from flask import Blueprint
 from flask import current_app
 from flask import Flask
@@ -322,13 +321,11 @@ def test_app_cli_has_app_context(app, runner):
         app = click.get_current_context().obj.load_app()
         # the loaded app should be the same as current_app
         same_app = current_app._get_current_object() is app
-        # only one app context should be pushed
-        stack_size = len(_app_ctx_stack._local.stack)
-        return same_app, stack_size, value
+        return same_app, value
 
     cli = FlaskGroup(create_app=lambda: app)
     result = runner.invoke(cli, ["check", "x"], standalone_mode=False)
-    assert result.return_value == (True, 1, True)
+    assert result.return_value == (True, True)
 
 
 def test_with_appcontext(runner):