diff --git a/packages/flutter_tools/lib/src/test/flutter_platform.dart b/packages/flutter_tools/lib/src/test/flutter_platform.dart
index 1e3e2b4a03..6260cc9aa8 100644
--- a/packages/flutter_tools/lib/src/test/flutter_platform.dart
+++ b/packages/flutter_tools/lib/src/test/flutter_platform.dart
@@ -15,6 +15,7 @@ import '../base/async_guard.dart';
 import '../base/common.dart';
 import '../base/file_system.dart';
 import '../base/io.dart';
+import '../base/process.dart';
 import '../build_info.dart';
 import '../cache.dart';
 import '../compile.dart';
@@ -307,6 +308,7 @@ class FlutterPlatform extends PlatformPlugin {
     this.testTimeRecorder,
     this.nativeAssetsBuilder,
     this.buildInfo,
+    this.shutdownHooks,
   });
 
   final String shellPath;
@@ -325,6 +327,7 @@ class FlutterPlatform extends PlatformPlugin {
   final TestTimeRecorder? testTimeRecorder;
   final TestCompilerNativeAssetsBuilder? nativeAssetsBuilder;
   final BuildInfo? buildInfo;
+  final ShutdownHooks? shutdownHooks;
 
   /// The device to run the test on for Integration Tests.
   ///
@@ -476,8 +479,35 @@ class FlutterPlatform extends PlatformPlugin {
 
     _AsyncError? outOfBandError; // error that we couldn't send to the harness that we need to send via our future
 
-    final List<Finalizer> finalizers = <Finalizer>[]; // Will be run in reverse order.
+    // Will be run in reverse order.
+    final List<Finalizer> finalizers = <Finalizer>[];
+    bool ranFinalizers = false;
     bool controllerSinkClosed = false;
+    Future<void> finalize() async {
+      if (ranFinalizers) {
+        return;
+      }
+      ranFinalizers = true;
+      globals.printTrace('test $ourTestCount: cleaning up...');
+      for (final Finalizer finalizer in finalizers.reversed) {
+        try {
+          await finalizer();
+        } on Exception catch (error, stack) {
+          globals.printTrace('test $ourTestCount: error while cleaning up; ${controllerSinkClosed ? "reporting to console" : "sending to test framework"}');
+          if (!controllerSinkClosed) {
+            testHarnessChannel.sink.addError(error, stack);
+          } else {
+            globals.printError('unhandled error during finalization of test:\n$testPath\n$error\n$stack');
+            outOfBandError ??= _AsyncError(error, stack);
+          }
+        }
+      }
+    }
+
+    // If the flutter CLI is forcibly terminated, cleanup processes.
+    final ShutdownHooks shutdownHooks = this.shutdownHooks ?? globals.shutdownHooks;
+    shutdownHooks.addShutdownHook(finalize);
+
     try {
       // Callback can't throw since it's just setting a variable.
       unawaited(testHarnessChannel.sink.done.whenComplete(() {
@@ -608,21 +638,7 @@ class FlutterPlatform extends PlatformPlugin {
         outOfBandError ??= _AsyncError(reportedError, reportedStackTrace);
       }
     } finally {
-      globals.printTrace('test $ourTestCount: cleaning up...');
-      // Finalizers are treated like a stack; run them in reverse order.
-      for (final Finalizer finalizer in finalizers.reversed) {
-        try {
-          await finalizer();
-        } on Exception catch (error, stack) {
-          globals.printTrace('test $ourTestCount: error while cleaning up; ${controllerSinkClosed ? "reporting to console" : "sending to test framework"}');
-          if (!controllerSinkClosed) {
-            testHarnessChannel.sink.addError(error, stack);
-          } else {
-            globals.printError('unhandled error during finalization of test:\n$testPath\n$error\n$stack');
-            outOfBandError ??= _AsyncError(error, stack);
-          }
-        }
-      }
+      await finalize();
       if (!controllerSinkClosed) {
         // Waiting below with await.
         unawaited(testHarnessChannel.sink.close());
diff --git a/packages/flutter_tools/test/general.shard/flutter_platform_test.dart b/packages/flutter_tools/test/general.shard/flutter_platform_test.dart
index 98c9afd81a..6a8d5fbfda 100644
--- a/packages/flutter_tools/test/general.shard/flutter_platform_test.dart
+++ b/packages/flutter_tools/test/general.shard/flutter_platform_test.dart
@@ -7,6 +7,7 @@ import 'package:flutter_tools/src/application_package.dart';
 import 'package:flutter_tools/src/base/file_system.dart';
 import 'package:flutter_tools/src/base/io.dart';
 import 'package:flutter_tools/src/base/logger.dart';
+import 'package:flutter_tools/src/base/process.dart';
 import 'package:flutter_tools/src/build_info.dart';
 import 'package:flutter_tools/src/device.dart';
 import 'package:flutter_tools/src/flutter_manifest.dart';
@@ -97,6 +98,35 @@ void main() {
       ApplicationPackageFactory: () => _FakeApplicationPackageFactory(),
     });
 
+    testUsingContext('a shutdown signal terminates the test device', () async {
+      final _WorkingDevice testDevice = _WorkingDevice();
+
+      final ShutdownHooks shutdownHooks = ShutdownHooks();
+      final FlutterPlatform flutterPlatform = FlutterPlatform(
+        debuggingOptions: DebuggingOptions.disabled(BuildInfo.debug),
+        shellPath: '/',
+        enableVmService: false,
+        integrationTestDevice: testDevice,
+        flutterProject: _FakeFlutterProject(),
+        host: InternetAddress.anyIPv4,
+        updateGoldens: false,
+        shutdownHooks: shutdownHooks,
+      );
+
+      await expectLater(
+        () => flutterPlatform.loadChannel('test1.dart', fakeSuitePlatform).stream.drain<void>(),
+        returnsNormally,
+      );
+
+      final BufferLogger logger = globals.logger as BufferLogger;
+      await shutdownHooks.runShutdownHooks(logger);
+      expect(logger.traceText, contains('test 0: ensuring test device is terminated.'));
+    }, overrides: <Type, Generator>{
+      FileSystem: () => fileSystem,
+      ProcessManager: () => FakeProcessManager.any(),
+      ApplicationPackageFactory: () => _FakeApplicationPackageFactory(),
+    });
+
     testUsingContext('installHook creates a FlutterPlatform', () {
       expect(() => installHook(
         shellPath: 'abc',
@@ -214,6 +244,25 @@ class _UnstartableDevice extends Fake implements Device {
   }
 }
 
+class _WorkingDevice extends Fake implements Device {
+  @override
+  Future<void> dispose() async {}
+
+  @override
+  Future<TargetPlatform> get targetPlatform => Future<TargetPlatform>.value(TargetPlatform.android);
+
+  @override
+  Future<bool> stopApp(ApplicationPackage? app, {String? userIdentifier}) async => true;
+
+  @override
+  Future<bool> uninstallApp(ApplicationPackage app, {String? userIdentifier}) async => true;
+
+  @override
+  Future<LaunchResult> startApp(covariant ApplicationPackage? package, {String? mainPath, String? route, required DebuggingOptions debuggingOptions, Map<String, Object?> platformArgs = const <String, Object>{}, bool prebuiltApplication = false, String? userIdentifier}) async {
+    return LaunchResult.succeeded(vmServiceUri: Uri.parse('http://127.0.0.1:12345/vmService'));
+  }
+}
+
 class _FakeFlutterProject extends Fake implements FlutterProject {
   @override
   FlutterManifest get manifest => FlutterManifest.empty(logger: BufferLogger.test());