diff --git a/tests/http/test_server.py b/tests/http/test_server.py
index a3ef4997..79fb6866 100644
--- a/tests/http/test_server.py
+++ b/tests/http/test_server.py
@@ -12,8 +12,8 @@ from mopidy.http import actor, handlers
 
 
 class HttpServerTest(tornado.testing.AsyncHTTPTestCase):
-    def get_app(self):
-        config = {
+    def get_config(self):
+        return {
             'http': {
                 'hostname': '127.0.0.1',
                 'port': 6680,
@@ -21,6 +21,8 @@ class HttpServerTest(tornado.testing.AsyncHTTPTestCase):
                 'zeroconf': '',
             }
         }
+
+    def get_app(self):
         core = mock.Mock()
         core.get_version = mock.MagicMock(name='get_version')
         core.get_version.return_value = mopidy.__version__
@@ -28,7 +30,7 @@ class HttpServerTest(tornado.testing.AsyncHTTPTestCase):
         apps = [dict(name='testapp')]
         statics = [dict(name='teststatic')]
 
-        http_frontend = actor.HttpFrontend(config=config, core=core)
+        http_frontend = actor.HttpFrontend(config=self.get_config(), core=core)
         http_frontend.apps = [{
             'name': 'mopidy',
             'factory': handlers.make_mopidy_app_factory(apps, statics),
@@ -57,6 +59,28 @@ class RootAppTest(HttpServerTest):
         self.assertEqual(response.headers['Cache-Control'], 'no-cache')
 
 
+class LegacyStaticDirAppTest(HttpServerTest):
+    def get_config(self):
+        config = super(LegacyStaticDirAppTest, self).get_config()
+        config['http']['static_dir'] = os.path.dirname(__file__)
+        return config
+
+    def test_should_return_index(self):
+        response = self.fetch('/', method='GET', follow_redirects=False)
+
+        self.assertEqual(response.code, 404, 'No index.html in this dir')
+
+    def test_should_return_static_files(self):
+        response = self.fetch('/test_server.py', method='GET')
+
+        self.assertIn(
+            'test_should_return_static_files',
+            tornado.escape.to_unicode(response.body))
+        self.assertEqual(
+            response.headers['X-Mopidy-Version'], mopidy.__version__)
+        self.assertEqual(response.headers['Cache-Control'], 'no-cache')
+
+
 class MopidyAppTest(HttpServerTest):
     def test_should_return_index(self):
         response = self.fetch('/mopidy/', method='GET')