diff --git a/django/contrib/staticfiles/handlers.py b/django/contrib/staticfiles/handlers.py
index 2ec6d07d71..0c85c1ce40 100644
--- a/django/contrib/staticfiles/handlers.py
+++ b/django/contrib/staticfiles/handlers.py
@@ -4,6 +4,7 @@ from urllib.request import url2pathname
 from django.conf import settings
 from django.contrib.staticfiles import utils
 from django.contrib.staticfiles.views import serve
+from django.core.handlers.exception import response_for_exception
 from django.core.handlers.wsgi import WSGIHandler, get_path_info
 
 
@@ -59,6 +60,7 @@ class StaticFilesHandler(WSGIHandler):
                 if settings.DEBUG:
                     from django.views import debug
                     return debug.technical_404_response(request, e)
+                return response_for_exception(request, e)
         return super().get_response(request)
 
     def __call__(self, environ, start_response):
diff --git a/tests/staticfiles_tests/test_management.py b/tests/staticfiles_tests/test_management.py
index 1472c7a488..74c7ef9fc6 100644
--- a/tests/staticfiles_tests/test_management.py
+++ b/tests/staticfiles_tests/test_management.py
@@ -16,7 +16,7 @@ from django.contrib.staticfiles.management.commands import (
 )
 from django.core.exceptions import ImproperlyConfigured
 from django.core.management import CommandError, call_command
-from django.test import override_settings
+from django.test import RequestFactory, override_settings
 from django.test.utils import extend_sys_path
 from django.utils import timezone
 from django.utils._os import symlinks_supported
@@ -44,6 +44,18 @@ class TestRunserver(StaticFilesTestCase):
             command.get_handler(use_static_handler=True, insecure_serving=True)
             self.assertEqual(mocked.call_count, 1)
 
+    def test_404_response(self):
+        command = runserver.Command()
+        handler = command.get_handler(use_static_handler=True, insecure_serving=True)
+        missing_static_file = os.path.join(settings.STATIC_URL, 'unknown.css')
+        req = RequestFactory().get(missing_static_file)
+        with override_settings(DEBUG=False):
+            response = handler.get_response(req)
+            self.assertEqual(response.status_code, 404)
+        with override_settings(DEBUG=True):
+            response = handler.get_response(req)
+            self.assertEqual(response.status_code, 404)
+
 
 class TestFindStatic(TestDefaults, CollectionTestCase):
     """