diff --git a/packages/flutter_tools/lib/src/base/user_messages.dart b/packages/flutter_tools/lib/src/base/user_messages.dart
index 780561311e..6ebaa13471 100644
--- a/packages/flutter_tools/lib/src/base/user_messages.dart
+++ b/packages/flutter_tools/lib/src/base/user_messages.dart
@@ -309,8 +309,8 @@ class UserMessages {
   String get runnerLocalEngineOrWebSdkRequired =>
       'You must specify --local-engine or --local-web-sdk if you are using a locally built engine or web sdk.';
   // TODO(matanlurey): Make this an error, https://github.com/flutter/flutter/issues/132245.
-  String get runnerLocalEngineRequiresHostEngine =>
-      'Warning! You are using a locally built engine (--local-engine) but have not specified --local-host-engine.\n'
+  String runnerLocalEngineRequiresHostEngine({bool warning = false}) =>
+      '${warning ? 'Warning! ' : ''}You are using a locally built engine (--local-engine) but have not specified --local-host-engine.\n'
       'You may be building with a different engine than the one you are running with. '
       'See https://github.com/flutter/flutter/issues/132245 for details (in the future this will become '
       'an error).';
diff --git a/packages/flutter_tools/lib/src/context_runner.dart b/packages/flutter_tools/lib/src/context_runner.dart
index a5a4f92c25..a3f0b268ab 100644
--- a/packages/flutter_tools/lib/src/context_runner.dart
+++ b/packages/flutter_tools/lib/src/context_runner.dart
@@ -276,6 +276,11 @@ Future<T> runInContext<T>(
         platform: globals.platform,
         fileSystem: globals.fs,
         flutterRoot: Cache.flutterRoot!,
+        // TODO(matanlurey): https://github.com/flutter/flutter/issues/132245.
+        // Even though we *think* this feature is stable, we'd like to verify
+        // that automated tests are all providing `--local-engine-host` before
+        // enforcing it for all users.
+        treatMissingLocalEngineHostAsFatal: runningOnBot,
       ),
       Logger: () => globals.platform.isWindows
         ? WindowsStdoutLogger(
diff --git a/packages/flutter_tools/lib/src/runner/local_engine.dart b/packages/flutter_tools/lib/src/runner/local_engine.dart
index 57c9c19a8b..5170bf59e2 100644
--- a/packages/flutter_tools/lib/src/runner/local_engine.dart
+++ b/packages/flutter_tools/lib/src/runner/local_engine.dart
@@ -33,17 +33,20 @@ class LocalEngineLocator {
     required FileSystem fileSystem,
     required String flutterRoot,
     required UserMessages userMessages,
+    bool treatMissingLocalEngineHostAsFatal = false,
   }) : _platform = platform,
        _logger = logger,
        _fileSystem = fileSystem,
        _flutterRoot = flutterRoot,
-        _userMessages = userMessages;
+        _userMessages = userMessages,
+        _treatMissingLocalEngineHostAsFatal = treatMissingLocalEngineHostAsFatal;
 
   final Platform _platform;
   final Logger _logger;
   final FileSystem _fileSystem;
   final String _flutterRoot;
   final UserMessages _userMessages;
+  final bool _treatMissingLocalEngineHostAsFatal;
 
   /// Returns the engine build path of a local engine if one is located, otherwise `null`.
   Future<EngineBuildPaths?> findEnginePath({
@@ -206,8 +209,11 @@ class LocalEngineLocator {
       }
 
       if (localHostEngine == null) {
-        // TODO(matanlurey): https://github.com/flutter/flutter/issues/132245, change to throwToolExit.
-        _logger.printStatus(_userMessages.runnerLocalEngineRequiresHostEngine);
+        // TODO(matanlurey): https://github.com/flutter/flutter/issues/132245, always throwToolExit.
+        if (_treatMissingLocalEngineHostAsFatal) {
+          throwToolExit(_userMessages.runnerLocalEngineRequiresHostEngine());
+        }
+        _logger.printStatus(_userMessages.runnerLocalEngineRequiresHostEngine(warning: true));
       }
       final String basename = localHostEngine ?? _fileSystem.path.basename(engineBuildPath);
       final String hostBasename = _getHostEngineBasename(basename);
diff --git a/packages/flutter_tools/test/commands.shard/hermetic/attach_test.dart b/packages/flutter_tools/test/commands.shard/hermetic/attach_test.dart
index 5740b20c93..d334c8aa9d 100644
--- a/packages/flutter_tools/test/commands.shard/hermetic/attach_test.dart
+++ b/packages/flutter_tools/test/commands.shard/hermetic/attach_test.dart
@@ -276,7 +276,7 @@ void main() {
           platform: platform,
           processInfo: processInfo,
           fileSystem: testFileSystem,
-        )).run(<String>['attach', '--local-engine-src-path=$localEngineSrc', '--local-engine=$localEngineDir']);
+        )).run(<String>['attach', '--local-engine-src-path=$localEngineSrc', '--local-engine=$localEngineDir', '--local-engine-host=$localEngineDir']);
         await Future.wait<void>(<Future<void>>[
           completer.future,
           fakeLogReader.dispose(),
diff --git a/packages/flutter_tools/test/general.shard/runner/local_engine_test.dart b/packages/flutter_tools/test/general.shard/runner/local_engine_test.dart
index f2f3aedcbf..b18a3633a2 100644
--- a/packages/flutter_tools/test/general.shard/runner/local_engine_test.dart
+++ b/packages/flutter_tools/test/general.shard/runner/local_engine_test.dart
@@ -145,6 +145,29 @@ void main() {
     expect(logger.statusText, contains('Warning! You are using a locally built engine (--local-engine) but have not specified --local-host-engine'));
   });
 
+  testWithoutContext('fails if --local-engine-host is emitted and treatMissingLocalEngineHostAsFatal is set', () async {
+    final FileSystem fileSystem = MemoryFileSystem.test();
+    final Directory localEngine = fileSystem
+        .directory('$kArbitraryEngineRoot/src/out/android_debug_unopt_arm64/')
+        ..createSync(recursive: true);
+    fileSystem.directory('$kArbitraryEngineRoot/src/out/host_debug_unopt/').createSync(recursive: true);
+
+    final BufferLogger logger = BufferLogger.test();
+    final LocalEngineLocator localEngineLocator = LocalEngineLocator(
+      fileSystem: fileSystem,
+      flutterRoot: 'flutter/flutter',
+      logger: logger,
+      userMessages: UserMessages(),
+      platform: FakePlatform(environment: <String, String>{}),
+      treatMissingLocalEngineHostAsFatal: true,
+    );
+
+    await expectLater(
+      localEngineLocator.findEnginePath(localEngine: localEngine.path),
+      throwsToolExit(message: 'You are using a locally built engine (--local-engine) but have not specified --local-host-engine'),
+    );
+  });
+
   testWithoutContext('works if --local-engine is specified and --local-engine-src-path '
       'is determined by --local-engine', () async {
     final FileSystem fileSystem = MemoryFileSystem.test();