diff --git a/packages/flutter_tools/lib/src/commands/debug_adapter.dart b/packages/flutter_tools/lib/src/commands/debug_adapter.dart
index 7b495c61d5a..8ebf3f83916 100644
--- a/packages/flutter_tools/lib/src/commands/debug_adapter.dart
+++ b/packages/flutter_tools/lib/src/commands/debug_adapter.dart
@@ -59,6 +59,14 @@ class DebugAdapterCommand extends FlutterCommand {
       ipv6: ipv6 ?? false,
       enableDds: enableDds,
       test: boolArgDeprecated('test'),
+      onError: (Object? e) {
+        globals.printError(
+          'Input could not be parsed as a Debug Adapter Protocol message.\n'
+          'The "flutter debug-adapter" command is intended for use by tooling '
+          'that communicates using the Debug Adapter Protocol.\n\n'
+          '$e',
+        );
+      },
     );
 
     await server.channel.closed;
diff --git a/packages/flutter_tools/lib/src/debug_adapters/flutter_adapter.dart b/packages/flutter_tools/lib/src/debug_adapters/flutter_adapter.dart
index f271f259ebf..256c2356eb4 100644
--- a/packages/flutter_tools/lib/src/debug_adapters/flutter_adapter.dart
+++ b/packages/flutter_tools/lib/src/debug_adapters/flutter_adapter.dart
@@ -28,6 +28,7 @@ class FlutterDebugAdapter extends DartDebugAdapter<FlutterLaunchRequestArguments
     bool enableDds = true,
     super.enableAuthCodes,
     super.logger,
+    super.onError,
   })  : _enableDds = enableDds,
         // Always disable in the DAP layer as it's handled in the spawned
         // 'flutter' process.
diff --git a/packages/flutter_tools/lib/src/debug_adapters/flutter_test_adapter.dart b/packages/flutter_tools/lib/src/debug_adapters/flutter_test_adapter.dart
index d7af0eb2089..2c682d25c6b 100644
--- a/packages/flutter_tools/lib/src/debug_adapters/flutter_test_adapter.dart
+++ b/packages/flutter_tools/lib/src/debug_adapters/flutter_test_adapter.dart
@@ -28,6 +28,7 @@ class FlutterTestDebugAdapter extends DartDebugAdapter<FlutterLaunchRequestArgum
     bool enableDds = true,
     super.enableAuthCodes,
     super.logger,
+    super.onError,
   })  : _enableDds = enableDds,
         // Always disable in the DAP layer as it's handled in the spawned
         // 'flutter' process.
diff --git a/packages/flutter_tools/lib/src/debug_adapters/server.dart b/packages/flutter_tools/lib/src/debug_adapters/server.dart
index 7780ea821cf..7c72307dbbb 100644
--- a/packages/flutter_tools/lib/src/debug_adapters/server.dart
+++ b/packages/flutter_tools/lib/src/debug_adapters/server.dart
@@ -30,21 +30,28 @@ class DapServer {
     this.enableAuthCodes = true,
     bool test = false,
     this.logger,
+    void Function(Object? e)? onError,
   }) : channel = ByteStreamServerChannel(input, output, logger) {
     adapter = test
-        ? FlutterTestDebugAdapter(channel,
+        ? FlutterTestDebugAdapter(
+            channel,
             fileSystem: fileSystem,
             platform: platform,
             ipv6: ipv6,
             enableDds: enableDds,
             enableAuthCodes: enableAuthCodes,
-            logger: logger)
-        : FlutterDebugAdapter(channel,
+            logger: logger,
+            onError: onError,
+          )
+        : FlutterDebugAdapter(
+            channel,
             fileSystem: fileSystem,
             platform: platform,
             enableDds: enableDds,
             enableAuthCodes: enableAuthCodes,
-            logger: logger);
+            logger: logger,
+            onError: onError,
+          );
   }
 
   final ByteStreamServerChannel channel;
diff --git a/packages/flutter_tools/test/integration.shard/debug_adapter/flutter_adapter_test.dart b/packages/flutter_tools/test/integration.shard/debug_adapter/flutter_adapter_test.dart
index 94294b7a4ff..0923e5e7432 100644
--- a/packages/flutter_tools/test/integration.shard/debug_adapter/flutter_adapter_test.dart
+++ b/packages/flutter_tools/test/integration.shard/debug_adapter/flutter_adapter_test.dart
@@ -8,6 +8,7 @@ import 'package:dds/dap.dart';
 import 'package:dds/src/dap/protocol_generated.dart';
 import 'package:file/file.dart';
 import 'package:flutter_tools/src/cache.dart';
+import 'package:flutter_tools/src/convert.dart';
 import 'package:flutter_tools/src/globals.dart' as globals;
 
 import '../../src/common.dart';
@@ -15,6 +16,7 @@ import '../test_data/basic_project.dart';
 import '../test_data/compile_error_project.dart';
 import '../test_utils.dart';
 import 'test_client.dart';
+import 'test_server.dart';
 import 'test_support.dart';
 
 void main() {
@@ -97,6 +99,27 @@ void main() {
       ]);
     });
 
+    testWithoutContext('outputs useful message on invalid DAP protocol messages', () async {
+      final OutOfProcessDapTestServer server = dap.server as OutOfProcessDapTestServer;
+      final CompileErrorProject project = CompileErrorProject();
+      await project.setUpIn(tempDir);
+
+      final StringBuffer stderrOutput = StringBuffer();
+      dap.server.onStderrOutput = stderrOutput.write;
+
+      // Write invalid headers and await the error.
+      dap.server.sink.add(utf8.encode('foo\r\nbar\r\n\r\n'));
+      await server.exitCode;
+
+      // Verify the user-friendly message was included in the output.
+      final String error = stderrOutput.toString();
+      expect(error, contains('Input could not be parsed as a Debug Adapter Protocol message'));
+      expect(error, contains('The "flutter debug-adapter" command is intended for use by tooling'));
+      // This test only runs with out-of-process DAP as it's testing _actual_
+      // stderr output and that the debug-adapter process terminates, which is
+      // not possible when running the DAP Server in-process.
+    }, skip: useInProcessDap); // [intended] See above.
+
     testWithoutContext('correctly outputs launch errors and terminates', () async {
       final CompileErrorProject project = CompileErrorProject();
       await project.setUpIn(tempDir);
diff --git a/packages/flutter_tools/test/integration.shard/debug_adapter/test_client.dart b/packages/flutter_tools/test/integration.shard/debug_adapter/test_client.dart
index 76c42d301dd..e1f823ad478 100644
--- a/packages/flutter_tools/test/integration.shard/debug_adapter/test_client.dart
+++ b/packages/flutter_tools/test/integration.shard/debug_adapter/test_client.dart
@@ -325,7 +325,7 @@ extension DapTestClientExtension on DapTestClient {
   Future<List<OutputEventBody>> collectAllOutput({
     String? program,
     String? cwd,
-    Future<Response> Function()? start,
+    Future<void> Function()? start,
     Future<Response> Function()? launch,
     bool skipInitialPubGetOutput = true
   }) async {
diff --git a/packages/flutter_tools/test/integration.shard/debug_adapter/test_server.dart b/packages/flutter_tools/test/integration.shard/debug_adapter/test_server.dart
index 43be68bf420..f92da208d41 100644
--- a/packages/flutter_tools/test/integration.shard/debug_adapter/test_server.dart
+++ b/packages/flutter_tools/test/integration.shard/debug_adapter/test_server.dart
@@ -19,6 +19,7 @@ abstract class DapTestServer {
   Future<void> stop();
   StreamSink<List<int>> get sink;
   Stream<List<int>> get stream;
+  Function(String message)? onStderrOutput;
 }
 
 /// An instance of a DAP server running in-process (to aid debugging).
@@ -73,22 +74,27 @@ class OutOfProcessDapTestServer extends DapTestServer {
     this._process,
     Logger? logger,
   ) {
-    // Treat anything written to stderr as the DAP crashing and fail the test
-    // unless it's "Waiting for another flutter command to release the startup
-    // lock" or we're tearing down.
+    // Unless we're given an error handler, treat anything written to stderr as
+    // the DAP crashing and fail the test unless it's "Waiting for another
+    // flutter command to release the startup lock" or we're tearing down.
     _process.stderr
         .transform(utf8.decoder)
         .where((String error) => !error.contains('Waiting for another flutter command to release the startup lock'))
         .listen((String error) {
       logger?.call(error);
       if (!_isShuttingDown) {
-        throw Exception(error);
+        final Function(String message)? stderrHandler = onStderrOutput;
+        if (stderrHandler != null) {
+          stderrHandler(error);
+        } else {
+          throw Exception(error);
+        }
       }
     });
     unawaited(_process.exitCode.then((int code) {
       final String message = 'Out-of-process DAP server terminated with code $code';
       logger?.call(message);
-      if (!_isShuttingDown && code != 0) {
+      if (!_isShuttingDown && code != 0 && onStderrOutput == null) {
         throw Exception(message);
       }
     }));
@@ -97,6 +103,8 @@ class OutOfProcessDapTestServer extends DapTestServer {
   bool _isShuttingDown = false;
   final Process _process;
 
+  Future<int> get exitCode => _process.exitCode;
+
   @override
   StreamSink<List<int>> get sink => _process.stdin;