diff --git a/packages/flutter_tools/lib/src/build_runner/resident_web_runner.dart b/packages/flutter_tools/lib/src/build_runner/resident_web_runner.dart
index 5eb6a41fccf..b7380fde589 100644
--- a/packages/flutter_tools/lib/src/build_runner/resident_web_runner.dart
+++ b/packages/flutter_tools/lib/src/build_runner/resident_web_runner.dart
@@ -20,8 +20,10 @@ import '../base/net.dart';
 import '../base/terminal.dart';
 import '../base/utils.dart';
 import '../build_info.dart';
+import '../cache.dart';
 import '../compile.dart';
 import '../convert.dart';
+import '../dart/pub.dart';
 import '../devfs.dart';
 import '../device.dart';
 import '../features.dart';
@@ -403,6 +405,14 @@ class _ResidentWebRunner extends ResidentWebRunner {
 
     try {
       return await asyncGuard(() async {
+        // Ensure dwds resources are cached. If the .packages file is missing then
+        // the client.js script cannot be located by the injected handler in dwds.
+        // This will result in a NoSuchMethodError thrown by injected_handler.darts
+        await pub.get(
+          context: PubContext.pubGet,
+          directory: globals.fs.path.join(Cache.flutterRoot, 'packages', 'flutter_tools')
+        );
+
         device.devFS = WebDevFS(
           hostname: effectiveHostname,
           port: hostPort,
diff --git a/packages/flutter_tools/test/general.shard/resident_web_runner_cold_test.dart b/packages/flutter_tools/test/general.shard/resident_web_runner_cold_test.dart
index 1a315bf49bb..9444d43fa2c 100644
--- a/packages/flutter_tools/test/general.shard/resident_web_runner_cold_test.dart
+++ b/packages/flutter_tools/test/general.shard/resident_web_runner_cold_test.dart
@@ -10,6 +10,7 @@ import 'package:flutter_tools/src/base/logger.dart';
 import 'package:flutter_tools/src/base/terminal.dart';
 import 'package:flutter_tools/src/build_info.dart';
 import 'package:flutter_tools/src/build_system/build_system.dart';
+import 'package:flutter_tools/src/dart/pub.dart';
 import 'package:flutter_tools/src/device.dart';
 import 'package:flutter_tools/src/globals.dart' as globals;
 import 'package:flutter_tools/src/project.dart';
@@ -54,7 +55,9 @@ void main() {
           stayResident: true,
           urlTunneller: null,
         ) as ResidentWebRunner;
-      },
+      }, overrides: <Type, Generator>{
+        Pub: () => MockPub(),
+      }
     );
   });
 
@@ -166,3 +169,4 @@ class MockChromeConnection extends Mock implements ChromeConnection {}
 class MockChromeTab extends Mock implements ChromeTab {}
 class MockWipConnection extends Mock implements WipConnection {}
 class MockBuildSystem extends Mock implements BuildSystem {}
+class MockPub extends Mock implements Pub {}
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 c460695c3fb..934e918e1e9 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
@@ -13,6 +13,7 @@ import 'package:flutter_tools/src/base/terminal.dart';
 import 'package:flutter_tools/src/build_info.dart';
 import 'package:flutter_tools/src/build_runner/resident_web_runner.dart';
 import 'package:flutter_tools/src/compile.dart';
+import 'package:flutter_tools/src/dart/pub.dart';
 import 'package:flutter_tools/src/devfs.dart';
 import 'package:flutter_tools/src/device.dart';
 import 'package:flutter_tools/src/globals.dart' as globals;
@@ -82,6 +83,9 @@ void main() {
         globals.fs.currentDirectory.childFile('.packages')
           .writeAsStringSync('\n');
       },
+      overrides: <Type, Generator>{
+        Pub: () => MockPub(),
+      }
     );
   });
 
@@ -214,6 +218,10 @@ void main() {
     verify(mockAppConnection.runMain()).called(1);
     verify(mockVmService.registerService('reloadSources', 'FlutterTools')).called(1);
     verify(status.stop()).called(1);
+    verify(pub.get(
+      context: PubContext.pubGet,
+      directory: globals.fs.path.join('packages', 'flutter_tools')
+    )).called(1);
 
     expect(bufferLogger.statusText, contains('Debug service listening on ws://127.0.0.1/abcd/'));
     expect(debugConnectionInfo.wsUri.toString(), 'ws://127.0.0.1/abcd/');
@@ -978,3 +986,4 @@ class MockWipConnection extends Mock implements WipConnection {}
 class MockWipDebugger extends Mock implements WipDebugger {}
 class MockWebServerDevice extends Mock implements WebServerDevice {}
 class MockDevice extends Mock implements Device {}
+class MockPub extends Mock implements Pub {}