diff --git a/packages/flutter_tools/lib/src/resident_runner.dart b/packages/flutter_tools/lib/src/resident_runner.dart
index 9c86abbcd8..a424873a9b 100644
--- a/packages/flutter_tools/lib/src/resident_runner.dart
+++ b/packages/flutter_tools/lib/src/resident_runner.dart
@@ -23,6 +23,7 @@ import 'base/utils.dart';
 import 'build_info.dart';
 import 'build_system/build_system.dart';
 import 'build_system/targets/localizations.dart';
+import 'bundle.dart';
 import 'cache.dart';
 import 'codegen.dart';
 import 'compile.dart';
@@ -83,6 +84,12 @@ class FlutterDevice {
     if (device.platformType == PlatformType.fuchsia) {
       targetModel = TargetModel.flutterRunner;
     }
+    // For both web and non-web platforms we initialize dill to/from
+    // a shared location for faster bootstrapping. If the compiler fails
+    // due to a kernel target or version mismatch, no error is reported
+    // and the compiler starts up as normal. Unexpected errors will print
+    // a warning message and dump some debug information which can be
+    // used to file a bug, but the compiler will still start up correctly.
     if (targetPlatform == TargetPlatform.web_javascript) {
       generator = ResidentCompiler(
         globals.artifacts.getArtifactPath(Artifact.flutterWebSdk, mode: buildInfo.mode),
@@ -95,6 +102,9 @@ class FlutterDevice {
         compilerMessageConsumer:
           (String message, {bool emphasis, TerminalColor color, }) =>
             globals.printTrace(message),
+        initializeFromDill: getDefaultCachedKernelPath(
+          trackWidgetCreation: buildInfo.trackWidgetCreation,
+        ),
         targetModel: TargetModel.dartdevc,
         experimentalFlags: experimentalFlags,
         platformDill: globals.fs.file(globals.artifacts
@@ -119,6 +129,9 @@ class FlutterDevice {
         targetModel: targetModel,
         experimentalFlags: experimentalFlags,
         dartDefines: buildInfo.dartDefines,
+        initializeFromDill: getDefaultCachedKernelPath(
+          trackWidgetCreation: buildInfo.trackWidgetCreation,
+        ),
         packagesPath: globalPackagesPath,
       );
     }
@@ -691,7 +704,6 @@ abstract class ResidentRunner {
   final bool ipv6;
   final String _dillOutputPath;
   /// The parent location of the incremental artifacts.
-  @visibleForTesting
   final Directory artifactDirectory;
   final String packagesFilePath;
   final String projectRootPath;
@@ -1196,6 +1208,12 @@ abstract class ResidentRunner {
   Future<void> preExit() async {
     // If _dillOutputPath is null, we created a temporary directory for the dill.
     if (_dillOutputPath == null && artifactDirectory.existsSync()) {
+      final File outputDill = globals.fs.file(dillOutputPath);
+      if (outputDill.existsSync()) {
+        outputDill.copySync(getDefaultCachedKernelPath(
+          trackWidgetCreation: trackWidgetCreation,
+        ));
+      }
       artifactDirectory.deleteSync(recursive: true);
     }
   }
diff --git a/packages/flutter_tools/test/general.shard/resident_runner_test.dart b/packages/flutter_tools/test/general.shard/resident_runner_test.dart
index 30c9e1e258..319df1a121 100644
--- a/packages/flutter_tools/test/general.shard/resident_runner_test.dart
+++ b/packages/flutter_tools/test/general.shard/resident_runner_test.dart
@@ -4,10 +4,10 @@
 
 import 'dart:async';
 
-import 'package:file_testing/file_testing.dart';
 import 'package:flutter_tools/src/cache.dart';
 import 'package:vm_service/vm_service.dart' as vm_service;
 import 'package:file/memory.dart';
+import 'package:file_testing/file_testing.dart';
 import 'package:flutter_tools/src/artifacts.dart';
 import 'package:flutter_tools/src/base/command_help.dart';
 import 'package:flutter_tools/src/base/common.dart';
@@ -521,6 +521,24 @@ void main() {
     expect(otherRunner.artifactDirectory.path, contains('foobar'));
   }));
 
+  test('ResidentRunner copies output dill to cache location during preExit', () => testbed.run(() async {
+    fakeVmServiceHost = FakeVmServiceHost(requests: <VmServiceExpectation>[]);
+    residentRunner.artifactDirectory.childFile('app.dill').writeAsStringSync('hello');
+    await residentRunner.preExit();
+    final File cacheDill = globals.fs.file(globals.fs.path.join(getBuildDirectory(), 'cache.dill'));
+
+    expect(cacheDill, exists);
+    expect(cacheDill.readAsStringSync(), 'hello');
+  }));
+
+  test('ResidentRunner handles output dill missing during preExit', () => testbed.run(() async {
+    fakeVmServiceHost = FakeVmServiceHost(requests: <VmServiceExpectation>[]);
+    await residentRunner.preExit();
+    final File cacheDill = globals.fs.file(globals.fs.path.join(getBuildDirectory(), 'cache.dill'));
+
+    expect(cacheDill, isNot(exists));
+  }));
+
   test('ResidentRunner can run source generation', () => testbed.run(() async {
     final FakeProcessManager processManager = globals.processManager as FakeProcessManager;
     final Directory dependencies = globals.fs.directory(
@@ -1140,6 +1158,8 @@ void main() {
       target: null,
     )).generator as DefaultResidentCompiler;
 
+    expect(residentCompiler.initializeFromDill,
+      globals.fs.path.join(getBuildDirectory(), 'cache.dill'));
     expect(residentCompiler.librariesSpec,
       globals.fs.file(globals.artifacts.getArtifactPath(Artifact.flutterWebLibrariesJson))
         .uri.toString());