diff --git a/readthedocs/proxito/middleware.py b/readthedocs/proxito/middleware.py
index 9f179583c0f..50cf96e4ac2 100644
--- a/readthedocs/proxito/middleware.py
+++ b/readthedocs/proxito/middleware.py
@@ -167,6 +167,28 @@ def process_request(self, request):  # noqa
         # Otherwise set the slug on the request
         request.host_project_slug = request.slug = ret
 
+        try:
+            project = Project.objects.get(slug=request.host_project_slug)
+        except Project.DoesNotExist:
+            log.exception('No host_project_slug set on project')
+            return None
+
+        # This is hacky because Django wants a module for the URLConf,
+        # instead of also accepting string
+        if project.urlconf:
+
+            # Stop Django from caching URLs
+            project_timestamp = project.modified_date.strftime("%Y%m%d.%H%M%S")
+            url_key = f'readthedocs.urls.fake.{project.slug}.{project_timestamp}'
+
+            log.info(
+                'Setting URLConf: project=%s url_key=%s urlconf=%s',
+                project, url_key, project.urlconf,
+            )
+            if url_key not in sys.modules:
+                sys.modules[url_key] = project.proxito_urlconf
+            request.urlconf = url_key
+
         return None
 
     def process_response(self, request, response):  # noqa