diff --git a/CHANGELOG.md b/CHANGELOG.md
index c3f4031e..fd9f9ff0 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -34,6 +34,10 @@ Using the following categories, list your changes in this order:
 
 ## [Unreleased](https://github.com/Archmonger/ServeStatic/compare/1.1.0...HEAD)
 
+### Added
+
+-   Verbose Django `404` error page when `settings.py:DEBUG` is `True` ([Upstream PR](https://github.com/evansd/whitenoise/pull/366))
+
 ### Fixed
 
 -   Fix compatibility with third-party sync only middleware
diff --git a/src/servestatic/middleware.py b/src/servestatic/middleware.py
index 52ee2ec4..66eca968 100644
--- a/src/servestatic/middleware.py
+++ b/src/servestatic/middleware.py
@@ -18,6 +18,8 @@
 from django.http import FileResponse
 from django.urls import get_script_prefix
 
+from servestatic.responders import MissingFileError
+
 from .asgi import BLOCK_SIZE
 from .string_utils import ensure_leading_trailing_slash
 from .wsgi import ServeStatic
@@ -175,6 +177,18 @@ async def __call__(self, request):
         if static_file is not None:
             return await self.aserve(static_file, request)
 
+        if settings.DEBUG and request.path.startswith(settings.STATIC_URL):
+            current_finders = finders.get_finders()
+            app_dirs = [
+                storage.location
+                for finder in current_finders
+                for storage in finder.storages.values()
+            ]
+            app_dirs = "\n• ".join(sorted(app_dirs))
+            raise MissingFileError(
+                f"ServeStatic did not find the file '{request.path.lstrip(settings.STATIC_URL)}' within the following paths:\n• {app_dirs}"
+            )
+
         return await self.get_response(request)
 
     @staticmethod
diff --git a/tests/django_urls.py b/tests/django_urls.py
index 562b8d6f..157b9b17 100644
--- a/tests/django_urls.py
+++ b/tests/django_urls.py
@@ -1,3 +1,10 @@
 from __future__ import annotations
 
-urlpatterns = []
+from django.urls import path
+
+
+def avoid_django_default_welcome_page():
+    pass
+
+
+urlpatterns = [path("", avoid_django_default_welcome_page)]
diff --git a/tests/test_django_whitenoise.py b/tests/test_django_whitenoise.py
index 590ddb70..3dfa862f 100644
--- a/tests/test_django_whitenoise.py
+++ b/tests/test_django_whitenoise.py
@@ -1,31 +1,33 @@
 from __future__ import annotations
 
 import asyncio
+import html
 import shutil
 import tempfile
 from contextlib import closing
-from urllib.parse import urljoin
-from urllib.parse import urlparse
+from pathlib import Path
+from urllib.parse import urljoin, urlparse
 
 import brotli
 import pytest
 from django.conf import settings
-from django.contrib.staticfiles import finders
-from django.contrib.staticfiles import storage
+from django.contrib.staticfiles import finders, storage
 from django.core.asgi import get_asgi_application
 from django.core.management import call_command
 from django.core.wsgi import get_wsgi_application
 from django.test.utils import override_settings
 from django.utils.functional import empty
 
-from .utils import AppServer
-from .utils import AsgiAppServer
-from .utils import AsgiReceiveEmulator
-from .utils import AsgiScopeEmulator
-from .utils import AsgiSendEmulator
-from .utils import Files
-from servestatic.middleware import ServeStaticFileResponse
-from servestatic.middleware import ServeStaticMiddleware
+from servestatic.middleware import ServeStaticFileResponse, ServeStaticMiddleware
+
+from .utils import (
+    AppServer,
+    AsgiAppServer,
+    AsgiReceiveEmulator,
+    AsgiScopeEmulator,
+    AsgiSendEmulator,
+    Files,
+)
 
 
 def reset_lazy_object(obj):
@@ -188,7 +190,7 @@ def test_file_served_from_static_dir(finder_static_files, finder_server):
 
 
 def test_non_ascii_requests_safely_ignored(finder_server):
-    response = finder_server.get(settings.STATIC_URL + "test\u263A")
+    response = finder_server.get(settings.STATIC_URL + "test\u263a")
     assert 404 == response.status_code
 
 
@@ -238,3 +240,32 @@ def test_relative_static_url(server, static_files, _collect_static):
         url = storage.staticfiles_storage.url(static_files.js_path)
         response = server.get(url)
         assert response.content == static_files.js_content
+
+
+def test_404_in_prod(server):
+    response = server.get(settings.STATIC_URL + "garbage")
+    response_content = str(response.content.decode())
+    response_content = html.unescape(response_content)
+
+    assert response.status_code == 404
+    assert (
+        "ServeStatic did not find the file 'garbage' within the following paths:"
+        not in response_content
+    )
+
+
+@override_settings(DEBUG=True)
+def test_error_message(server):
+    response = server.get(f"{settings.STATIC_URL}garbage")
+    response_content = str(response.content.decode())
+    response_content = html.unescape(response_content)
+
+    # Beautify for easier debugging
+    response_content = response_content[response_content.index("ServeStatic") :]
+
+    assert (
+        "ServeStatic did not find the file 'garbage' within the following paths:"
+        in response_content
+    )
+    assert "•" in response_content
+    assert str(Path(__file__).parent / "test_files" / "static") in response_content