diff --git a/qutebrowser/config/configfiles.py b/qutebrowser/config/configfiles.py
index aab210bf1..7be756b2d 100644
--- a/qutebrowser/config/configfiles.py
+++ b/qutebrowser/config/configfiles.py
@@ -348,6 +348,9 @@ def read_config_py(filename, raising=False):
         raising: Raise exceptions happening in config.py.
                  This is needed during tests to use pytest's inspection.
     """
+    assert config.instance is not None
+    assert config.key_instance is not None
+
     api = ConfigAPI(config.instance, config.key_instance)
     container = config.ConfigContainer(config.instance, configapi=api)
     basename = os.path.basename(filename)
diff --git a/tests/unit/config/test_configfiles.py b/tests/unit/config/test_configfiles.py
index cef035a1f..6339784e9 100644
--- a/tests/unit/config/test_configfiles.py
+++ b/tests/unit/config/test_configfiles.py
@@ -273,14 +273,15 @@ class ConfPy:
                    'qbmodule.run(config)')
 
 
+@pytest.fixture
+def confpy(tmpdir, config_tmpdir, data_tmpdir, config_stub, key_config_stub):
+    return ConfPy(tmpdir)
+
+
 class TestConfigPyModules:
 
     pytestmark = pytest.mark.usefixtures('config_stub', 'key_config_stub')
 
-    @pytest.fixture
-    def confpy(self, tmpdir, config_tmpdir, data_tmpdir):
-        return ConfPy(tmpdir)
-
     @pytest.fixture
     def qbmodulepy(self, tmpdir):
         return ConfPy(tmpdir, filename="qbmodule.py")
@@ -342,10 +343,6 @@ class TestConfigPy:
 
     pytestmark = pytest.mark.usefixtures('config_stub', 'key_config_stub')
 
-    @pytest.fixture
-    def confpy(self, tmpdir, config_tmpdir, data_tmpdir):
-        return ConfPy(tmpdir)
-
     def test_assertions(self, confpy):
         """Make sure assertions in config.py work for these tests."""
         confpy.write('assert False')
@@ -660,6 +657,21 @@ class TestConfigPyWriter:
         lines = pyfile.read_text('utf-8').splitlines()
         assert '# Autogenerated config.py' in lines
 
+    def test_defaults_work(self, confpy):
+        """Get a config.py with default values and run it."""
+        options = [(opt, opt.default)
+                   for _name, opt in sorted(configdata.DATA.items())]
+        bindings = dict(configdata.DATA['bindings.default'].default)
+        writer = configfiles.ConfigPyWriter(options, bindings, commented=False)
+        writer.write(confpy.filename)
+
+        try:
+            configfiles.read_config_py(confpy.filename)
+        except configexc.ConfigFileErrors as exc:
+            # Make sure no other errors happened
+            for error in exc.errors:
+                assert isinstance(error.exception, configexc.BackendError)
+
 
 @pytest.fixture
 def init_patch(qapp, fake_save_manager, config_tmpdir, data_tmpdir,