diff --git a/dwds/CHANGELOG.md b/dwds/CHANGELOG.md
index b81c8d3db..6cfd966c0 100644
--- a/dwds/CHANGELOG.md
+++ b/dwds/CHANGELOG.md
@@ -12,6 +12,7 @@
   restart.
 - Remove verbose printing on receiving DevTools events.
 - Update `vm_service` version to `^8.2.0`.
+- Migrate .packages to package_config.json.
 - Update error message on expression evaluation using unloaded libraries.
 
 **Breaking changes:**
diff --git a/dwds/lib/src/readers/frontend_server_asset_reader.dart b/dwds/lib/src/readers/frontend_server_asset_reader.dart
index c44cedb0b..f11616208 100644
--- a/dwds/lib/src/readers/frontend_server_asset_reader.dart
+++ b/dwds/lib/src/readers/frontend_server_asset_reader.dart
@@ -37,8 +37,8 @@ class FrontendServerAssetReader implements AssetReader {
   /// Corresponding `.json` and `.map` files will be read relative to
   /// [outputPath].
   ///
-  /// [_packageRoot] is the path to the directory that contains a `.packages`
-  /// file for the application.
+  /// [_packageRoot] is the path to the directory that contains a
+  /// `.dart_tool/package_config.json` file for the application.
   FrontendServerAssetReader(
     String outputPath,
     this._packageRoot,
@@ -46,8 +46,8 @@ class FrontendServerAssetReader implements AssetReader {
         _mapIncremental = File('$outputPath.incremental.map'),
         _jsonOriginal = File('$outputPath.json'),
         _jsonIncremental = File('$outputPath.incremental.json'),
-        _packageConfig = loadPackageConfig(
-            File(p.absolute(p.join(_packageRoot, '.packages'))));
+        _packageConfig = loadPackageConfig(File(p
+            .absolute(p.join(_packageRoot, '.dart_tool/package_config.json'))));
 
   @override
   Future<String> dartSourceContents(String serverPath) async {
diff --git a/dwds/lib/src/utilities/dart_uri.dart b/dwds/lib/src/utilities/dart_uri.dart
index 4d3fb35cf..9903950af 100644
--- a/dwds/lib/src/utilities/dart_uri.dart
+++ b/dwds/lib/src/utilities/dart_uri.dart
@@ -157,7 +157,8 @@ class DartUri {
   /// Record library and script uris to enable resolving library and script paths.
   static Future<void> initialize(SdkConfiguration sdkConfiguration) async {
     _sdkConfiguration = sdkConfiguration;
-    var packagesUri = p.toUri(p.join(currentDirectory, '.packages'));
+    var packagesUri =
+        p.toUri(p.join(currentDirectory, '.dart_tool/package_config.json'));
 
     clear();
 
@@ -190,8 +191,8 @@ class DartUri {
   /// Returns the dirname for the server URI.
   static String _dirForServerUri(String uri) => p.dirname(Uri.parse(uri).path);
 
-  /// Load the .packages file associated with the running application so we can
-  /// resolve file URLs into package: URLs appropriately.
+  /// Load the .dart_tool/package_config.json file associated with the running
+  /// application so we can resolve file URLs into package: URLs appropriately.
   static Future<void> _loadPackageConfig(Uri uri) async {
     _packageConfig = await loadPackageConfigUri(uri, onError: (e) {
       _logger.warning('Cannot read packages spec: $uri', e);
diff --git a/dwds/test/fixtures/context.dart b/dwds/test/fixtures/context.dart
index e0b483713..b6395054a 100644
--- a/dwds/test/fixtures/context.dart
+++ b/dwds/test/fixtures/context.dart
@@ -98,11 +98,17 @@ class TestContext {
         .absolute(directory ?? p.relative(relativeDirectory, from: p.current)));
 
     DartUri.currentDirectory = workingDirectory;
-    _packagesFilePath = p.join(workingDirectory, '.packages');
+    _packagesFilePath =
+        p.join(workingDirectory, '.dart_tool/package_config.json');
 
-    _entryFile = File(p.normalize(
-        p.absolute(entry ?? p.relative(relativeEntry, from: p.current))));
+    var entryFilePath = p.normalize(
+        p.absolute(entry ?? p.relative(relativeEntry, from: p.current)));
 
+    _logger.info('Serving: $pathToServe/$path');
+    _logger.info('Packages: $_packagesFilePath');
+    _logger.info('Entry: $entryFilePath');
+
+    _entryFile = File(entryFilePath);
     _entryContents = _entryFile.readAsStringSync();
   }
 
@@ -241,15 +247,14 @@ class TestContext {
         case CompilationMode.frontendServer:
           {
             soundNullSafety ??= true;
-            var fileSystemRoot = p.dirname(_packagesFilePath);
+            var projectDirectory = p.dirname(p.dirname(_packagesFilePath));
             var entryPath =
-                _entryFile.path.substring(fileSystemRoot.length + 1);
+                _entryFile.path.substring(projectDirectory.length + 1);
             webRunner = ResidentWebRunner(
                 '${Uri.file(entryPath)}',
                 urlEncoder,
-                fileSystemRoot,
                 _packagesFilePath,
-                [fileSystemRoot],
+                [projectDirectory],
                 'org-dartlang-app',
                 _outputDir.path,
                 verboseCompiler);
diff --git a/dwds/test/frontend_server_breakpoint_test.dart b/dwds/test/frontend_server_breakpoint_test.dart
index cd0a8a2c5..54cfe877b 100644
--- a/dwds/test/frontend_server_breakpoint_test.dart
+++ b/dwds/test/frontend_server_breakpoint_test.dart
@@ -15,6 +15,7 @@ import 'package:vm_service/vm_service.dart';
 import 'package:webkit_inspection_protocol/webkit_inspection_protocol.dart';
 
 import 'fixtures/context.dart';
+import 'fixtures/logging.dart';
 
 final context = TestContext(
     directory: p.join('..', 'fixtures', '_testPackage'),
@@ -27,10 +28,22 @@ ChromeProxyService get service =>
 WipConnection get tabConnection => context.tabConnection;
 
 void main() {
+  // Enable verbose logging for debugging.
+  var debug = false;
+
+  // Change to 'true' to print expression compiler messages to console.
+  //
+  // Note: expression compiler runs in an isolate, so its output is not
+  // currently redirected to a logger. As a result, it will be printed
+  // regardless of the logger settings.
+  var verboseCompiler = false;
+
   group('shared context', () {
     setUpAll(() async {
+      setCurrentLogWriter(debug: debug);
       await context.setUp(
         compilationMode: CompilationMode.frontendServer,
+        verboseCompiler: verboseCompiler,
       );
     });
 
@@ -46,6 +59,7 @@ void main() {
       Stream<Event> stream;
 
       setUp(() async {
+        setCurrentLogWriter(debug: debug);
         vm = await service.getVM();
         isolate = await service.getIsolate(vm.isolates.first.id);
         scripts = await service.getScripts(isolate.id);
diff --git a/frontend_server_common/lib/src/asset_server.dart b/frontend_server_common/lib/src/asset_server.dart
index 756d489f7..776e35e6a 100644
--- a/frontend_server_common/lib/src/asset_server.dart
+++ b/frontend_server_common/lib/src/asset_server.dart
@@ -27,7 +27,7 @@ class TestAssetServer implements AssetReader {
   TestAssetServer(
     this._root,
     this._httpServer,
-    this._packages,
+    this._packageConfig,
     this.internetAddress,
     this._fileSystem,
   );
@@ -47,14 +47,12 @@ class TestAssetServer implements AssetReader {
     String hostname,
     int port,
     UrlEncoder urlTunneller,
+    PackageConfig packageConfig,
   ) async {
     var address = (await InternetAddress.lookup(hostname)).first;
     var httpServer = await HttpServer.bind(address, port);
-    var packages = await loadPackageConfigUri(Uri.base.resolve('.packages'),
-        loader: (Uri uri) => fileSystem.file(uri).readAsBytes());
     var server =
-        TestAssetServer(root, httpServer, packages, address, fileSystem);
-
+        TestAssetServer(root, httpServer, packageConfig, address, fileSystem);
     return server;
   }
 
@@ -64,8 +62,7 @@ class TestAssetServer implements AssetReader {
   final Map<String, Uint8List> _sourcemaps = <String, Uint8List>{};
   final Map<String, Uint8List> _metadata = <String, Uint8List>{};
   String _mergedMetadata;
-  // ignore: deprecated_member_use
-  final PackageConfig _packages;
+  final PackageConfig _packageConfig;
   final InternetAddress internetAddress;
 
   Uint8List getFile(String path) => _files[path];
@@ -241,7 +238,7 @@ class TestAssetServer implements AssetReader {
     // The file might have been a package file which is signaled by a
     // `/packages/<package>/<path>` request.
     if (segments.first == 'packages') {
-      var packageFile = _fileSystem.file(_packages
+      var packageFile = _fileSystem.file(_packageConfig
           .resolve(Uri(scheme: 'package', pathSegments: segments.skip(1))));
       if (packageFile.existsSync()) {
         return packageFile;
diff --git a/frontend_server_common/lib/src/devfs.dart b/frontend_server_common/lib/src/devfs.dart
index 568d1fad1..df097a498 100644
--- a/frontend_server_common/lib/src/devfs.dart
+++ b/frontend_server_common/lib/src/devfs.dart
@@ -12,6 +12,7 @@ import 'package:dwds/dwds.dart';
 import 'package:file/file.dart';
 import 'package:logging/logging.dart';
 import 'package:meta/meta.dart';
+import 'package:package_config/package_config.dart';
 import 'package:path/path.dart' as p;
 
 import 'asset.dart';
@@ -30,8 +31,7 @@ class WebDevFS {
     this.fileSystem,
     this.hostname,
     this.port,
-    this.packagesFilePath,
-    this.packagesPath,
+    this.packageConfigPath,
     this.root,
     this.urlTunneller,
   });
@@ -40,24 +40,31 @@ class WebDevFS {
   TestAssetServer assetServer;
   final String hostname;
   final int port;
-  final String packagesFilePath;
-  final String packagesPath;
+  final String packageConfigPath;
   final String root;
   final UrlEncoder urlTunneller;
   Directory _savedCurrentDirectory;
   List<Uri> sources;
+  PackageConfig _packageConfig;
 
   Future<Uri> create() async {
     _savedCurrentDirectory = fileSystem.currentDirectory;
-    fileSystem.currentDirectory = packagesPath;
+    // package_config.json is located in <project directory>/.dart_tool/package_config
+    var projectDirectory = p.dirname(p.dirname(packageConfigPath));
+
+    fileSystem.currentDirectory = projectDirectory;
+
+    _packageConfig = await loadPackageConfigUri(Uri.file(packageConfigPath),
+        loader: (Uri uri) => fileSystem.file(uri).readAsBytes());
+
     assetServer = await TestAssetServer.start(
-        fileSystem, root, hostname, port, urlTunneller);
+        fileSystem, root, hostname, port, urlTunneller, _packageConfig);
     return Uri.parse('http://$hostname:$port');
   }
 
   Future<void> dispose() {
     fileSystem.currentDirectory = _savedCurrentDirectory;
-    return assetServer.close();
+    return assetServer?.close();
   }
 
   Future<UpdateFSReport> update({
@@ -102,11 +109,9 @@ class WebDevFS {
     generator.reset();
 
     var compilerOutput = await generator.recompile(
-      'org-dartlang-app:///$mainPath',
-      invalidatedFiles,
-      outputPath: p.join(dillOutputPath, 'app.dill'),
-      packagesFilePath: packagesFilePath,
-    );
+        Uri.parse('org-dartlang-app:///$mainPath'), invalidatedFiles,
+        outputPath: p.join(dillOutputPath, 'app.dill'),
+        packageConfig: _packageConfig);
     if (compilerOutput == null || compilerOutput.errorCount > 0) {
       return UpdateFSReport(success: false);
     }
diff --git a/frontend_server_common/lib/src/frontend_server_client.dart b/frontend_server_common/lib/src/frontend_server_client.dart
index 91ed7ffad..68f9a236b 100644
--- a/frontend_server_common/lib/src/frontend_server_client.dart
+++ b/frontend_server_common/lib/src/frontend_server_client.dart
@@ -158,68 +158,6 @@ class StdoutHandler {
   }
 }
 
-/// Converts filesystem paths to package URIs.
-class PackageUriMapper {
-  PackageUriMapper(String scriptPath, String packagesFilePath,
-      String fileSystemScheme, List<String> fileSystemRoots) {
-    init(scriptPath, packagesFilePath, fileSystemScheme, fileSystemRoots);
-  }
-
-  Future<void> init(String scriptPath, String packagesFilePath,
-      String fileSystemScheme, List<String> fileSystemRoots) async {
-    var packageConfig = await loadPackageConfig(
-        File(fileSystem.path.absolute(packagesFilePath)));
-    var isWindowsPath =
-        Platform.isWindows && !scriptPath.startsWith('org-dartlang-app');
-    var scriptUri = Uri.file(scriptPath, windows: isWindowsPath).toString();
-    for (var package in packageConfig.packages) {
-      var prefix = package.packageUriRoot.toString();
-      // Only perform a multi-root mapping if there are multiple roots.
-      if (fileSystemScheme != null &&
-          fileSystemRoots != null &&
-          fileSystemRoots.length > 1 &&
-          prefix.contains(fileSystemScheme)) {
-        _packageName = package.name;
-        _uriPrefixes = fileSystemRoots
-            .map((String name) =>
-                Uri.file(name, windows: Platform.isWindows).toString())
-            .toList();
-        return;
-      }
-      if (scriptUri.startsWith(prefix)) {
-        _packageName = package.name;
-        _uriPrefixes = <String>[prefix];
-        return;
-      }
-    }
-  }
-
-  String _packageName;
-  List<String> _uriPrefixes;
-
-  Uri map(String scriptPath) {
-    if (_packageName == null) {
-      return null;
-    }
-    var scriptUri =
-        Uri.file(scriptPath, windows: Platform.isWindows).toString();
-    for (var uriPrefix in _uriPrefixes) {
-      if (scriptUri.startsWith(uriPrefix)) {
-        return Uri.parse(
-            'package:$_packageName/${scriptUri.substring(uriPrefix.length)}');
-      }
-    }
-    return null;
-  }
-
-  static Uri findUri(String scriptPath, String packagesFilePath,
-      String fileSystemScheme, List<String> fileSystemRoots) {
-    return PackageUriMapper(
-            scriptPath, packagesFilePath, fileSystemScheme, fileSystemRoots)
-        .map(scriptPath);
-  }
-}
-
 /// Class that allows to serialize compilation requests to the compiler.
 abstract class _CompilationRequest {
   _CompilationRequest(this.completer);
@@ -236,16 +174,16 @@ abstract class _CompilationRequest {
 class _RecompileRequest extends _CompilationRequest {
   _RecompileRequest(
     Completer<CompilerOutput> completer,
-    this.mainPath,
+    this.mainUri,
     this.invalidatedFiles,
     this.outputPath,
-    this.packagesFilePath,
+    this.packageConfig,
   ) : super(completer);
 
-  String mainPath;
+  Uri mainUri;
   List<Uri> invalidatedFiles;
   String outputPath;
-  String packagesFilePath;
+  PackageConfig packageConfig;
 
   @override
   Future<CompilerOutput> _run(DefaultResidentCompiler compiler) async =>
@@ -316,7 +254,7 @@ class _RejectRequest extends _CompilationRequest {
 abstract class ResidentCompiler {
   factory ResidentCompiler(
     String sdkRoot, {
-    String packagesPath,
+    String packageConfigPath,
     List<String> fileSystemRoots,
     String fileSystemScheme,
     String platformDill,
@@ -330,18 +268,14 @@ abstract class ResidentCompiler {
   void addFileSystemRoot(String root);
 
   /// If invoked for the first time, it compiles Dart script identified by
-  /// [mainPath], [invalidatedFiles] list is ignored.
+  /// [mainUri], [invalidatedFiles] list is ignored.
   /// On successive runs [invalidatedFiles] indicates which files need to be
-  /// recompiled. If [mainPath] is null, previously used [mainPath] entry
+  /// recompiled. If [mainUri] is null, previously used [mainUri] entry
   /// point that is used for recompilation.
   /// Binary file name is returned if compilation was successful, otherwise
   /// null is returned.
-  Future<CompilerOutput> recompile(
-    String mainPath,
-    List<Uri> invalidatedFiles, {
-    @required String outputPath,
-    String packagesFilePath,
-  });
+  Future<CompilerOutput> recompile(Uri mainUri, List<Uri> invalidatedFiles,
+      {@required String outputPath, @required PackageConfig packageConfig});
 
   Future<CompilerOutput> compileExpression(
     String expression,
@@ -387,7 +321,7 @@ abstract class ResidentCompiler {
 class DefaultResidentCompiler implements ResidentCompiler {
   DefaultResidentCompiler(
     String sdkRoot, {
-    this.packagesPath,
+    this.packageConfigPath,
     this.fileSystemRoots,
     this.fileSystemScheme,
     this.platformDill,
@@ -398,7 +332,7 @@ class DefaultResidentCompiler implements ResidentCompiler {
         // This is a URI, not a file path, so the forward slash is correct even on Windows.
         sdkRoot = sdkRoot.endsWith('/') ? sdkRoot : '$sdkRoot/';
 
-  final String packagesPath;
+  final String packageConfigPath;
   final List<String> fileSystemRoots;
   final String fileSystemScheme;
   final String platformDill;
@@ -420,8 +354,9 @@ class DefaultResidentCompiler implements ResidentCompiler {
       StreamController<_CompilationRequest>();
 
   @override
-  Future<CompilerOutput> recompile(String mainPath, List<Uri> invalidatedFiles,
-      {@required String outputPath, String packagesFilePath}) async {
+  Future<CompilerOutput> recompile(Uri mainUri, List<Uri> invalidatedFiles,
+      {@required String outputPath,
+      @required PackageConfig packageConfig}) async {
     assert(outputPath != null);
     if (!_controller.hasListener) {
       _controller.stream.listen(_handleCompilationRequest);
@@ -429,40 +364,34 @@ class DefaultResidentCompiler implements ResidentCompiler {
 
     var completer = Completer<CompilerOutput>();
     _controller.add(_RecompileRequest(
-        completer, mainPath, invalidatedFiles, outputPath, packagesFilePath));
+        completer, mainUri, invalidatedFiles, outputPath, packageConfig));
     return completer.future;
   }
 
   Future<CompilerOutput> _recompile(_RecompileRequest request) async {
     _stdoutHandler.reset();
 
-    // First time recompile is called we actually have to compile the app from
-    // scratch ignoring list of invalidated files.
-    PackageUriMapper packageUriMapper;
-    if (request.packagesFilePath != null) {
-      packageUriMapper = PackageUriMapper(
-        request.mainPath,
-        request.packagesFilePath,
-        fileSystemScheme,
-        fileSystemRoots,
-      );
-    }
+    final mainUri =
+        request.packageConfig.toPackageUri(request.mainUri)?.toString() ??
+            toMultiRootPath(request.mainUri, fileSystemScheme, fileSystemRoots);
 
     _compileRequestNeedsConfirmation = true;
 
     if (_server == null) {
-      return _compile(_mapFilename(request.mainPath, packageUriMapper),
-          request.outputPath, request.packagesFilePath);
+      return _compile(mainUri, request.outputPath);
     }
 
     var inputKey = Uuid().generateV4();
-    var mainUri = request.mainPath != null
-        ? '${_mapFilename(request.mainPath, packageUriMapper)} '
-        : '';
     _server.stdin.writeln('recompile $mainUri$inputKey');
     _logger.info('<- recompile $mainUri$inputKey');
     for (var fileUri in request.invalidatedFiles) {
-      var message = _mapFileUri(fileUri.toString(), packageUriMapper);
+      String message;
+      if (fileUri.scheme == 'package') {
+        message = fileUri.toString();
+      } else {
+        message = request.packageConfig.toPackageUri(fileUri)?.toString() ??
+            toMultiRootPath(fileUri, fileSystemScheme, fileSystemRoots);
+      }
       _server.stdin.writeln(message);
       _logger.info(message);
     }
@@ -490,7 +419,7 @@ class DefaultResidentCompiler implements ResidentCompiler {
   }
 
   Future<CompilerOutput> _compile(
-      String scriptUri, String outputFilePath, String packagesFilePath) async {
+      String scriptUri, String outputFilePath) async {
     var frontendServer = frontendServerExecutable;
     var args = <String>[
       frontendServer,
@@ -501,12 +430,9 @@ class DefaultResidentCompiler implements ResidentCompiler {
       '-Ddart.developer.causal_async_stacks=true',
       '--output-dill',
       outputFilePath,
-      if (packagesFilePath != null) ...<String>[
+      if (packageConfigPath != null) ...<String>[
         '--packages',
-        packagesFilePath,
-      ] else if (packagesPath != null) ...<String>[
-        '--packages',
-        packagesPath,
+        packageConfigPath,
       ],
       if (fileSystemRoots != null)
         for (final String root in fileSystemRoots) ...<String>[
@@ -527,8 +453,9 @@ class DefaultResidentCompiler implements ResidentCompiler {
     ];
 
     _logger.info(args.join(' '));
+    var projectDirectory = p.dirname(p.dirname(packageConfigPath));
     _server = await Process.start(Platform.resolvedExecutable, args,
-        workingDirectory: packagesPath);
+        workingDirectory: projectDirectory);
     _server.stdout
         .transform<String>(utf8.decoder)
         .transform<String>(const LineSplitter())
@@ -693,46 +620,6 @@ class DefaultResidentCompiler implements ResidentCompiler {
     return _server.exitCode;
   }
 
-  String _mapFilename(String filename, PackageUriMapper packageUriMapper) {
-    return _doMapFilename(filename, packageUriMapper) ?? filename;
-  }
-
-  String _mapFileUri(String fileUri, PackageUriMapper packageUriMapper) {
-    String filename;
-    try {
-      filename = Uri.parse(fileUri).toFilePath();
-    } on UnsupportedError catch (_) {
-      return fileUri;
-    }
-    return _doMapFilename(filename, packageUriMapper) ?? fileUri;
-  }
-
-  String _doMapFilename(String filename, PackageUriMapper packageUriMapper) {
-    if (packageUriMapper != null) {
-      var packageUri = packageUriMapper.map(filename);
-      if (packageUri != null) {
-        return packageUri.toString();
-      }
-    }
-
-    if (fileSystemRoots != null) {
-      for (var root in fileSystemRoots) {
-        if (filename.startsWith(root)) {
-          return Uri(
-                  scheme: fileSystemScheme,
-                  path: filename.substring(root.length))
-              .toString();
-        }
-      }
-    }
-    if (Platform.isWindows &&
-        fileSystemRoots != null &&
-        fileSystemRoots.length > 1) {
-      return Uri.file(filename, windows: Platform.isWindows).toString();
-    }
-    return null;
-  }
-
   @override
   Future<dynamic> shutdown() async {
     // Server was never successfully created.
@@ -788,3 +675,20 @@ class TestExpressionCompiler implements ExpressionCompiler {
   @override
   Future<void> initialize({String moduleFormat, bool soundNullSafety}) async {}
 }
+
+/// Convert a file URI into a multi-root scheme URI if provided, otherwise
+/// return unmodified.
+@visibleForTesting
+String toMultiRootPath(
+    Uri fileUri, String scheme, List<String> fileSystemRoots) {
+  if (scheme == null || fileSystemRoots.isEmpty || fileUri.scheme != 'file') {
+    return fileUri.toString();
+  }
+  final filePath = fileUri.toFilePath(windows: Platform.isWindows);
+  for (final fileSystemRoot in fileSystemRoots) {
+    if (filePath.startsWith(fileSystemRoot)) {
+      return '$scheme://${filePath.substring(fileSystemRoot.length)}';
+    }
+  }
+  return fileUri.toString();
+}
diff --git a/frontend_server_common/lib/src/resident_runner.dart b/frontend_server_common/lib/src/resident_runner.dart
index 9f14f8704..ed692f8ea 100644
--- a/frontend_server_common/lib/src/resident_runner.dart
+++ b/frontend_server_common/lib/src/resident_runner.dart
@@ -28,14 +28,13 @@ class ResidentWebRunner {
   ResidentWebRunner(
       this.mainPath,
       this.urlTunneller,
-      this.packagesPath,
-      this.packagesFilePath,
+      this.packageConfigPath,
       this.fileSystemRoots,
       this.fileSystemScheme,
       this.outputPath,
       bool verbose) {
     generator = ResidentCompiler(dartSdkPath,
-        packagesPath: packagesPath,
+        packageConfigPath: packageConfigPath,
         platformDill: '$platformDill',
         fileSystemRoots: fileSystemRoots,
         fileSystemScheme: fileSystemScheme,
@@ -45,8 +44,7 @@ class ResidentWebRunner {
 
   final UrlEncoder urlTunneller;
   final String mainPath;
-  final String packagesPath;
-  final String packagesFilePath;
+  final String packageConfigPath;
   final String outputPath;
   final List<String> fileSystemRoots;
   final String fileSystemScheme;
@@ -67,8 +65,7 @@ class ResidentWebRunner {
       fileSystem: fileSystem,
       hostname: hostname,
       port: port,
-      packagesFilePath: packagesFilePath,
-      packagesPath: packagesPath,
+      packageConfigPath: packageConfigPath,
       root: root,
       urlTunneller: urlTunneller,
     );
diff --git a/webdev/test/e2e_test.dart b/webdev/test/e2e_test.dart
index e5779b2b9..b5a47980b 100644
--- a/webdev/test/e2e_test.dart
+++ b/webdev/test/e2e_test.dart
@@ -53,7 +53,9 @@ void main() {
 
     await process.shouldExit(0);
 
-    await d.file('.packages', isNotEmpty).validate(exampleDirectory);
+    await d
+        .file('.dart_tool/package_config.json', isNotEmpty)
+        .validate(exampleDirectory);
     await d.file('pubspec.lock', isNotEmpty).validate(exampleDirectory);
   });
 
diff --git a/webdev/test/integration_test.dart b/webdev/test/integration_test.dart
index 259ed60f8..be766da1b 100644
--- a/webdev/test/integration_test.dart
+++ b/webdev/test/integration_test.dart
@@ -53,9 +53,9 @@ name: sample
             ))
         .create();
 
-    await d.file('.packages', '''
-''').create();
     await d.dir('.dart_tool', [d.file('package_config.json', '')]).create();
+    await d.file('.dart_tool/package_config.json', '''
+''').create();
 
     var process = await runWebDev(['serve'], workingDirectory: d.sandbox);
 
@@ -84,10 +84,10 @@ name: sample
               .file('pubspec.lock', _pubspecLock(runnerVersion: null))
               .create();
 
-          await d.file('.packages', '''
-''').create();
           await d
               .dir('.dart_tool', [d.file('package_config.json', '')]).create();
+          await d.file('.dart_tool/package_config.json', '''
+''').create();
 
           var process = await runWebDev([command], workingDirectory: d.sandbox);
 
@@ -107,10 +107,10 @@ name: sample
               .file('pubspec.lock', _pubspecLock(webCompilersVersion: null))
               .create();
 
-          await d.file('.packages', '''
-''').create();
           await d
               .dir('.dart_tool', [d.file('package_config.json', '')]).create();
+          await d.file('.dart_tool/package_config.json', '''
+''').create();
 
           var process = await runWebDev(['serve'], workingDirectory: d.sandbox);
 
@@ -132,10 +132,10 @@ name: sample
               .file('pubspec.lock', _pubspecLock(webCompilersVersion: null))
               .create();
 
-          await d.file('.packages', '''
-''').create();
           await d
               .dir('.dart_tool', [d.file('package_config.json', '')]).create();
+          await d.file('.dart_tool/package_config.json', '''
+''').create();
 
           // Required for webdev to not complain about nothing to serve.
           await d.dir('web').create();
@@ -184,10 +184,10 @@ name: sample
                           daemonVersion: buildDaemonVersion))
                   .create();
 
-              await d.file('.packages', '''
-''').create();
               await d.dir(
                   '.dart_tool', [d.file('package_config.json', '')]).create();
+              await d.file('.dart_tool/package_config.json', '''
+''').create();
 
               var process =
                   await runWebDev(['serve'], workingDirectory: d.sandbox);
@@ -240,8 +240,8 @@ name: sample
       test('should fail if there has been a dependency change', () async {
         await d.file('pubspec.lock', _pubspecLock()).create();
 
-        await d.file('.packages', '').create();
         await d.dir('.dart_tool', [d.file('package_config.json', '')]).create();
+        await d.file('.dart_tool/package_config.json', '').create();
 
         // Ensure there is a noticeable delta in the creation times
         await Future.delayed(const Duration(milliseconds: 1100));