diff --git a/CHANGELOG.txt b/CHANGELOG.txt
index 92410fc8c0c..fdf4f1e039e 100644
--- a/CHANGELOG.txt
+++ b/CHANGELOG.txt
@@ -28,6 +28,8 @@
 * Fixed a bug in which the placeholder cache was not consistently cleared when a page was published.
 * Enhanced the plugin menu to not show plugins the user does not have permission to add.
 * Fixed a regression which prevented users from setting a redirect to the homepage.
+* Fixed a ``ValueError`` raised when using ``ManifestStaticFilesStorage`` or similar for static files.
+  This only affects Django >= 1.10
 
 
 === 3.4.3 (2017-04-24) ===
diff --git a/cms/templatetags/cms_static.py b/cms/templatetags/cms_static.py
index 05c79575f0c..18da36119de 100644
--- a/cms/templatetags/cms_static.py
+++ b/cms/templatetags/cms_static.py
@@ -28,5 +28,7 @@ def do_static_with_version(parser, token):
 class StaticWithVersionNode(StaticNode):
 
     def url(self, context):
-        url = super(StaticWithVersionNode, self).url(context)
-        return static_with_version(url)
+        path = self.path.resolve(context)
+        path_with_version = static_with_version(path)
+
+        return self.handle_simple(path_with_version)
diff --git a/cms/tests/test_templatetags.py b/cms/tests/test_templatetags.py
index f470e74f867..3495afbbb31 100644
--- a/cms/tests/test_templatetags.py
+++ b/cms/tests/test_templatetags.py
@@ -10,6 +10,7 @@
 from django.core import mail
 from django.core.exceptions import ImproperlyConfigured
 from django.test import RequestFactory
+from django.test.utils import override_settings
 from django.utils.html import escape
 from django.utils.timezone import now
 from djangocms_text_ckeditor.cms_plugins import TextPlugin
@@ -17,6 +18,8 @@
 from sekizai.data import UniqueSequence
 from sekizai.helpers import get_varname
 
+from mock import patch
+
 import cms
 from cms.api import create_page, create_title, add_plugin
 from cms.middleware.toolbar import ToolbarMiddleware
@@ -100,6 +103,31 @@ def test_static_with_version(self):
         output = self.render_template_obj(template, {}, None)
         self.assertEqual(expected, output)
 
+    @override_settings(STATICFILES_STORAGE='django.contrib.staticfiles.storage.ManifestStaticFilesStorage')
+    @patch('django.contrib.staticfiles.storage.staticfiles_storage')
+    def test_static_with_version_manifest(self, mock_storage):
+        """
+        Check that static files are looked up at the location where they are
+        stored when using static file manifests.
+        """
+        mock_storage.url.side_effect = lambda x: '/static/' + x
+
+        template = (
+            """{% load staticfiles cms_static %}<script src="{% static_with_version "cms/css/cms.base.css" %}" """
+            """type="text/javascript"></script>"""
+        )
+
+        output = self.render_template_obj(template, {}, None)
+        # If the manifest is used for looking up the static file (Django 1.10
+        # and later), it needs to be looked up with a proper path.
+        versioned_filename = 'cms/css/%s/cms.base.css' % cms.__version__
+        if mock_storage.url.called:
+            mock_storage.url.assert_called_with(versioned_filename)
+
+        expected = '<script src="/static/%s" type="text/javascript"></script>'
+        expected = expected % versioned_filename
+        self.assertEqual(expected, output)
+
 
 class TemplatetagDatabaseTests(TwoPagesFixture, CMSTestCase):
     def _getfirst(self):