diff --git a/webdev/lib/src/command/configuration.dart b/webdev/lib/src/command/configuration.dart
index 07f532261..e3036c384 100644
--- a/webdev/lib/src/command/configuration.dart
+++ b/webdev/lib/src/command/configuration.dart
@@ -38,6 +38,7 @@ const disableDdsFlag = 'disable-dds';
 const enableExperimentOption = 'enable-experiment';
 const canaryFeaturesFlag = 'canary';
 const offlineFlag = 'offline';
+const spaFallbackFlag = 'spa-fallback';
 
 ReloadConfiguration _parseReloadConfiguration(ArgResults argResults) {
   var auto = argResults.options.contains(autoOption)
@@ -109,6 +110,7 @@ class Configuration {
   final List<String>? _experiments;
   final bool? _canaryFeatures;
   final bool? _offline;
+  final bool? _spaFallback;
 
   Configuration({
     bool? autoRun,
@@ -136,6 +138,7 @@ class Configuration {
     List<String>? experiments,
     bool? canaryFeatures,
     bool? offline,
+    bool? spaFallback,
   })  : _autoRun = autoRun,
         _chromeDebugPort = chromeDebugPort,
         _debugExtension = debugExtension,
@@ -158,7 +161,8 @@ class Configuration {
         _nullSafety = nullSafety,
         _experiments = experiments,
         _canaryFeatures = canaryFeatures,
-        _offline = offline {
+        _offline = offline,
+        _spaFallback = spaFallback {
     _validateConfiguration();
   }
 
@@ -234,7 +238,8 @@ class Configuration {
       nullSafety: other._nullSafety ?? _nullSafety,
       experiments: other._experiments ?? _experiments,
       canaryFeatures: other._canaryFeatures ?? _canaryFeatures,
-      offline: other._offline ?? _offline);
+      offline: other._offline ?? _offline,
+      spaFallback: other._spaFallback ?? _spaFallback);
 
   factory Configuration.noInjectedClientDefaults() =>
       Configuration(autoRun: false, debug: false, debugExtension: false);
@@ -291,6 +296,8 @@ class Configuration {
 
   bool get offline => _offline ?? false;
 
+  bool get spaFallback => _spaFallback ?? false;
+
   /// Returns a new configuration with values updated from the parsed args.
   static Configuration fromArgs(ArgResults? argResults,
       {Configuration? defaultConfiguration}) {
@@ -419,6 +426,10 @@ class Configuration {
         ? argResults[offlineFlag] as bool?
         : defaultConfiguration.verbose;
 
+    final spaFallback = argResults.options.contains(spaFallbackFlag)
+        ? argResults[spaFallbackFlag] as bool?
+        : defaultConfiguration.spaFallback;
+
     return Configuration(
       autoRun: defaultConfiguration.autoRun,
       chromeDebugPort: chromeDebugPort,
@@ -445,6 +456,7 @@ class Configuration {
       experiments: experiments,
       canaryFeatures: canaryFeatures,
       offline: offline,
+      spaFallback: spaFallback,
     );
   }
 }
diff --git a/webdev/lib/src/command/serve_command.dart b/webdev/lib/src/command/serve_command.dart
index 3c32817e8..c2337f19b 100644
--- a/webdev/lib/src/command/serve_command.dart
+++ b/webdev/lib/src/command/serve_command.dart
@@ -75,6 +75,10 @@ refresh: Performs a full page refresh.
     ..addFlag(logRequestsFlag,
         negatable: false,
         help: 'Enables logging for each request to the server.')
+    ..addFlag('spa-fallback',
+        negatable: false,
+        help: 'Serves index.html for any 404 from a non-asset request. '
+            'Useful for single-page applications with client-side routing.')
     ..addOption(tlsCertChainFlag,
         help:
             'The file location to a TLS Certificate to create an HTTPs server.\n'
diff --git a/webdev/lib/src/serve/webdev_server.dart b/webdev/lib/src/serve/webdev_server.dart
index e166503f6..48f7c5582 100644
--- a/webdev/lib/src/serve/webdev_server.dart
+++ b/webdev/lib/src/serve/webdev_server.dart
@@ -195,6 +195,43 @@ class WebDevServer {
       cascade = cascade.add(assetHandler);
     }
 
+    if (options.configuration.spaFallback) {
+      FutureOr<Response> spaFallbackHandler(Request request) async {
+        final hasExt = request.url.pathSegments.isNotEmpty &&
+            request.url.pathSegments.last.contains('.');
+        if (request.method != 'GET' || hasExt) {
+          return Response.notFound('Not Found');
+        }
+
+        final indexUri =
+            request.requestedUri.replace(path: 'index.html', query: '');
+
+        final cleanHeaders = Map.of(request.headers)
+          ..remove('if-none-match')
+          ..remove('if-modified-since');
+
+        final proxiedReq = Request(
+          'GET',
+          indexUri,
+          headers: cleanHeaders,
+          context: request.context,
+          protocolVersion: request.protocolVersion,
+        );
+
+        final resp = await assetHandler(proxiedReq);
+
+        if (resp.statusCode != 200 && resp.statusCode != 304) {
+          return Response.notFound('Not Found');
+        }
+        return resp.change(headers: {
+          ...resp.headers,
+          'content-type': 'text/html; charset=utf-8',
+        });
+      }
+
+      cascade = cascade.add(spaFallbackHandler);
+    }
+
     final hostname = options.configuration.hostname;
     final tlsCertChain = options.configuration.tlsCertChain ?? '';
     final tlsCertKey = options.configuration.tlsCertKey ?? '';