diff --git a/packages/flutter_tools/lib/src/isolated/devfs_web.dart b/packages/flutter_tools/lib/src/isolated/devfs_web.dart
index 79a33a7298..bcaa2e368d 100644
--- a/packages/flutter_tools/lib/src/isolated/devfs_web.dart
+++ b/packages/flutter_tools/lib/src/isolated/devfs_web.dart
@@ -179,7 +179,7 @@ class WebAssetServer implements AssetReader {
   static Future<WebAssetServer> start(
     ChromiumLauncher? chromiumLauncher,
     String hostname,
-    int? port,
+    int port,
     UrlTunneller? urlTunneller,
     bool useSseForDebugProxy,
     bool useSseForDebugBackend,
@@ -203,7 +203,7 @@ class WebAssetServer implements AssetReader {
     const int kMaxRetries = 4;
     for (int i = 0; i <= kMaxRetries; i++) {
       try {
-        httpServer = await HttpServer.bind(address, port ?? await globals.os.findFreePort());
+        httpServer = await HttpServer.bind(address, port);
         break;
       } on SocketException catch (e, s) {
         if (i >= kMaxRetries) {
@@ -638,7 +638,7 @@ class WebDevFS implements DevFS {
   /// server.
   WebDevFS({
     required this.hostname,
-    required int? port,
+    required int port,
     required this.packagesFilePath,
     required this.urlTunneller,
     required this.useSseForDebugProxy,
@@ -671,7 +671,7 @@ class WebDevFS implements DevFS {
   final ChromiumLauncher? chromiumLauncher;
   final bool nullAssertions;
   final bool nativeNullAssertions;
-  final int? _port;
+  final int _port;
   final NullSafetyMode nullSafetyMode;
 
   late WebAssetServer webAssetServer;
diff --git a/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart b/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart
index 035fe08862..f7bb791061 100644
--- a/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart
+++ b/packages/flutter_tools/lib/src/isolated/resident_web_runner.dart
@@ -28,6 +28,7 @@ import '../dart/language_version.dart';
 import '../devfs.dart';
 import '../device.dart';
 import '../flutter_plugins.dart';
+import '../globals.dart' as globals;
 import '../project.dart';
 import '../reporting/reporting.dart';
 import '../resident_devtools_handler.dart';
@@ -254,15 +255,38 @@ class ResidentWebRunner extends ResidentRunner {
 
     try {
       return await asyncGuard(() async {
+        Future<int> getPort() async {
+          if (debuggingOptions.port == null) {
+            return globals.os.findFreePort();
+          }
+
+          final int? port = int.tryParse(debuggingOptions.port ?? '');
+
+          if (port == null) {
+            logger.printError('''
+Received a non-integer value for port: ${debuggingOptions.port}
+A randomly-chosen available port will be used instead.
+''');
+            return globals.os.findFreePort();
+          }
+
+          if (port < 0 || port > 65535) {
+            throwToolExit('''
+Invalid port: ${debuggingOptions.port}
+Please provide a valid TCP port (an integer between 0 and 65535, inclusive).
+    ''');
+          }
+
+          return port;
+        }
+
         final ExpressionCompiler? expressionCompiler =
           debuggingOptions.webEnableExpressionEvaluation
               ? WebExpressionCompiler(device!.generator!, fileSystem: _fileSystem)
               : null;
         device!.devFS = WebDevFS(
           hostname: debuggingOptions.hostname ?? 'localhost',
-          port: debuggingOptions.port != null
-            ? int.tryParse(debuggingOptions.port!)
-            : null,
+          port: await getPort(),
           packagesFilePath: packagesFilePath,
           urlTunneller: _urlTunneller,
           useSseForDebugProxy: debuggingOptions.webUseSseForDebugProxy,
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 f601a3b48c..acd6c09d86 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
@@ -1311,6 +1311,23 @@ flutter:
     FileSystem: () => fileSystem,
     ProcessManager: () => processManager,
   });
+
+  testUsingContext('throws when port is an integer outside the valid TCP range', () async {
+    final BufferLogger logger = BufferLogger.test();
+
+    DebuggingOptions debuggingOptions = DebuggingOptions.enabled(BuildInfo.debug, port: '65536');
+    ResidentRunner residentWebRunner =
+        setUpResidentRunner(flutterDevice, logger: logger, debuggingOptions: debuggingOptions);
+    await expectToolExitLater(residentWebRunner.run(), matches('Invalid port: 65536.*'));
+
+    debuggingOptions = DebuggingOptions.enabled(BuildInfo.debug, port: '-1');
+    residentWebRunner =
+      setUpResidentRunner(flutterDevice, logger: logger, debuggingOptions: debuggingOptions);
+    await expectToolExitLater(residentWebRunner.run(), matches('Invalid port: -1.*'));
+  }, overrides: <Type, Generator>{
+    FileSystem: () => fileSystem,
+    ProcessManager: () => processManager,
+  });
 }
 
 ResidentRunner setUpResidentRunner(