diff --git a/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart b/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart
index 9cca8f7021f..a3a32e79c83 100644
--- a/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart
+++ b/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart
@@ -174,10 +174,8 @@ class ResidentWebRunner extends ResidentRunner {
       debuggingOptions.buildInfo.ddcModuleFormat != DdcModuleFormat.ddc ||
       debuggingOptions.buildInfo.canaryFeatures != true;
 
-  // TODO(srujzs): Return true when web supports detaching.
-  // https://github.com/flutter/flutter/issues/163329
   @override
-  bool get supportsDetach => false;
+  bool get supportsDetach => stopAppDuringCleanup;
 
   ConnectionResult? _connectionResult;
   StreamSubscription<vmservice.Event>? _stdOutSub;
@@ -220,7 +218,11 @@ class ResidentWebRunner extends ResidentRunner {
     await _stdErrSub?.cancel();
     await _serviceSub?.cancel();
     await _extensionEventSub?.cancel();
-    await device!.device!.stopApp(null);
+
+    if (stopAppDuringCleanup) {
+      await device!.device!.stopApp(null);
+    }
+
     _registeredMethodsForService.clear();
     try {
       _generatedEntrypointDirectory?.deleteSync(recursive: true);
@@ -808,7 +810,9 @@ Please provide a valid TCP port (an integer between 0 and 65535, inclusive).
 
   @override
   Future<void> exitApp() async {
-    await device!.exitApps();
+    if (stopAppDuringCleanup) {
+      await device!.exitApps();
+    }
     appFinished();
   }
 
diff --git a/packages/flutter_tools/lib/src/resident_runner.dart b/packages/flutter_tools/lib/src/resident_runner.dart
index 1fb6909f60e..185201281fa 100644
--- a/packages/flutter_tools/lib/src/resident_runner.dart
+++ b/packages/flutter_tools/lib/src/resident_runner.dart
@@ -970,9 +970,6 @@ abstract class ResidentHandlers {
   Future<void> cleanupAfterSignal();
 
   /// Tear down the runner and leave the application running.
-  ///
-  /// This is not supported on web devices where the runner is running
-  /// the application server as well.
   Future<void> detach();
 
   /// Tear down the runner and exit the application.
diff --git a/packages/flutter_tools/test/general.shard/resident_web_runner_test.dart b/packages/flutter_tools/test/general.shard/resident_web_runner_test.dart
index 5fef0e13540..f3c4ecde757 100644
--- a/packages/flutter_tools/test/general.shard/resident_web_runner_test.dart
+++ b/packages/flutter_tools/test/general.shard/resident_web_runner_test.dart
@@ -405,6 +405,90 @@ void main() {
     },
   );
 
+  testUsingContext(
+    'Detach keeps device running',
+    () async {
+      final BufferLogger logger = BufferLogger.test();
+      fakeVmServiceHost = FakeVmServiceHost(requests: kAttachExpectations.toList());
+      setupMocks();
+      fileSystem.directory('web').deleteSync(recursive: true);
+      final ResidentWebRunner residentWebRunner = ResidentWebRunner(
+        flutterDevice,
+        flutterProject: FlutterProject.fromDirectoryTest(fileSystem.currentDirectory),
+        debuggingOptions: DebuggingOptions.enabled(BuildInfo.debug),
+        fileSystem: fileSystem,
+        logger: logger,
+        terminal: Terminal.test(),
+        platform: FakePlatform(),
+        outputPreferences: OutputPreferences.test(),
+        analytics: globals.analytics,
+        systemClock: globals.systemClock,
+        devtoolsHandler: createNoOpHandler,
+      );
+
+      mockDevice.dds = DartDevelopmentService(logger: logger);
+
+      expect(mockDevice.isRunning, false);
+      final Completer<DebugConnectionInfo> connectionInfoCompleter =
+          Completer<DebugConnectionInfo>();
+      unawaited(residentWebRunner.run(connectionInfoCompleter: connectionInfoCompleter));
+      await connectionInfoCompleter.future;
+      expect(mockDevice.isRunning, true);
+      await residentWebRunner.detach();
+      expect(residentWebRunner.stopAppDuringCleanup, false);
+      await residentWebRunner.exit();
+      await residentWebRunner.cleanupAtFinish();
+      expect(mockDevice.isRunning, true);
+    },
+    overrides: <Type, Generator>{
+      FileSystem: () => fileSystem,
+      ProcessManager: () => processManager,
+      FeatureFlags: enableExplicitPackageDependencies,
+      Pub: FakePubWithPrimedDeps.new,
+    },
+  );
+
+  testUsingContext(
+    'Quit stops device',
+    () async {
+      final BufferLogger logger = BufferLogger.test();
+      fakeVmServiceHost = FakeVmServiceHost(requests: kAttachExpectations.toList());
+      setupMocks();
+      fileSystem.directory('web').deleteSync(recursive: true);
+      final ResidentWebRunner residentWebRunner = ResidentWebRunner(
+        flutterDevice,
+        flutterProject: FlutterProject.fromDirectoryTest(fileSystem.currentDirectory),
+        debuggingOptions: DebuggingOptions.enabled(BuildInfo.debug),
+        fileSystem: fileSystem,
+        logger: logger,
+        terminal: Terminal.test(),
+        platform: FakePlatform(),
+        outputPreferences: OutputPreferences.test(),
+        analytics: globals.analytics,
+        systemClock: globals.systemClock,
+        devtoolsHandler: createNoOpHandler,
+      );
+
+      mockDevice.dds = DartDevelopmentService(logger: logger);
+
+      expect(mockDevice.isRunning, false);
+      final Completer<DebugConnectionInfo> connectionInfoCompleter =
+          Completer<DebugConnectionInfo>();
+      unawaited(residentWebRunner.run(connectionInfoCompleter: connectionInfoCompleter));
+      await connectionInfoCompleter.future;
+      expect(mockDevice.isRunning, true);
+      expect(residentWebRunner.stopAppDuringCleanup, true);
+      await residentWebRunner.cleanupAtFinish();
+      expect(mockDevice.isRunning, false);
+    },
+    overrides: <Type, Generator>{
+      FileSystem: () => fileSystem,
+      ProcessManager: () => processManager,
+      FeatureFlags: enableExplicitPackageDependencies,
+      Pub: FakePubWithPrimedDeps.new,
+    },
+  );
+
   testUsingContext(
     'Listens to stdout and stderr streams before running main',
     () async {
@@ -1593,6 +1677,8 @@ class FakeDevice extends Fake implements Device {
 
   int count = 0;
 
+  bool isRunning = false;
+
   @override
   Future<String> get sdkNameAndVersion async => 'SDK Name and Version';
 
@@ -1613,6 +1699,7 @@ class FakeDevice extends Fake implements Device {
     bool ipv6 = false,
     String? userIdentifier,
   }) async {
+    isRunning = true;
     return LaunchResult.succeeded();
   }
 
@@ -1622,6 +1709,7 @@ class FakeDevice extends Fake implements Device {
       throw StateError('stopApp called more than once.');
     }
     count += 1;
+    isRunning = false;
     return true;
   }
 }