diff --git a/packages/flutter_tools/lib/src/drive/web_driver_service.dart b/packages/flutter_tools/lib/src/drive/web_driver_service.dart
index 8958a4150b..a0b5c7296a 100644
--- a/packages/flutter_tools/lib/src/drive/web_driver_service.dart
+++ b/packages/flutter_tools/lib/src/drive/web_driver_service.dart
@@ -78,6 +78,7 @@ class WebDriverService extends DriverService {
           hostname: debuggingOptions.hostname,
           webRenderer: debuggingOptions.webRenderer,
           webUseWasm: debuggingOptions.webUseWasm,
+          webHeaders: debuggingOptions.webHeaders,
         )
         : DebuggingOptions.enabled(
           buildInfo,
@@ -86,6 +87,7 @@ class WebDriverService extends DriverService {
           disablePortPublication: debuggingOptions.disablePortPublication,
           webRenderer: debuggingOptions.webRenderer,
           webUseWasm: debuggingOptions.webUseWasm,
+          webHeaders: debuggingOptions.webHeaders,
         ),
       stayResident: true,
       flutterProject: FlutterProject.current(),
diff --git a/packages/flutter_tools/test/general.shard/drive/web_driver_service_test.dart b/packages/flutter_tools/test/general.shard/drive/web_driver_service_test.dart
index 8854e2c7a6..9d08262a09 100644
--- a/packages/flutter_tools/test/general.shard/drive/web_driver_service_test.dart
+++ b/packages/flutter_tools/test/general.shard/drive/web_driver_service_test.dart
@@ -270,6 +270,17 @@ void main() {
     WebRunnerFactory: () => FakeWebRunnerFactory(),
   });
 
+  testUsingContext('WebDriverService starts an app with provided web headers', () async {
+    final WebDriverService service = setUpDriverService();
+    final FakeDevice device = FakeDevice();
+    final Map<String, String> webHeaders = <String, String>{'test-header': 'test-value'};
+    await service.start(BuildInfo.profile, device, DebuggingOptions.enabled(BuildInfo.profile, webHeaders: webHeaders, ipv6: true));
+    await service.stop();
+    expect(FakeResidentRunner.instance.debuggingOptions.webHeaders, equals(webHeaders));
+  }, overrides: <Type, Generator>{
+    WebRunnerFactory: () => FakeWebRunnerFactory(),
+  });
+
   testUsingContext('WebDriverService will throw when an invalid launch url is provided', () async {
     final WebDriverService service = setUpDriverService();
     final FakeDevice device = FakeDevice();
@@ -310,7 +321,7 @@ class FakeWebRunnerFactory implements WebRunnerFactory {
     bool? stayResident,
     FlutterProject? flutterProject,
     bool? ipv6,
-    DebuggingOptions? debuggingOptions,
+    required DebuggingOptions debuggingOptions,
     UrlTunneller? urlTunneller,
     Logger? logger,
     FileSystem? fileSystem,
@@ -322,6 +333,7 @@ class FakeWebRunnerFactory implements WebRunnerFactory {
     expect(stayResident, isTrue);
     return FakeResidentRunner(
       doResolveToError: doResolveToError,
+      debuggingOptions: debuggingOptions,
     );
   }
 }
@@ -329,6 +341,7 @@ class FakeWebRunnerFactory implements WebRunnerFactory {
 class FakeResidentRunner extends Fake implements ResidentRunner {
   FakeResidentRunner({
     required this.doResolveToError,
+    required this.debuggingOptions,
   }) {
     instance = this;
   }
@@ -336,6 +349,8 @@ class FakeResidentRunner extends Fake implements ResidentRunner {
   static late FakeResidentRunner instance;
 
   final bool doResolveToError;
+  @override
+  final DebuggingOptions debuggingOptions;
   final Completer<int> _exitCompleter = Completer<int>();
   final List<String> callLog = <String>[];