diff --git a/lms/djangoapps/courseware/tests/test_comprehensive_theming.py b/lms/djangoapps/courseware/tests/test_comprehensive_theming.py
index e6702ab9ea..475bc33762 100644
--- a/lms/djangoapps/courseware/tests/test_comprehensive_theming.py
+++ b/lms/djangoapps/courseware/tests/test_comprehensive_theming.py
@@ -6,6 +6,7 @@ from django.test import TestCase
 from path import path           # pylint: disable=no-name-in-module
 from django.contrib import staticfiles
 
+import edxmako
 from openedx.core.djangoapps.theming.tests.test_util import with_comprehensive_theme
 from openedx.core.lib.tempdir import mkdtemp_clean, create_symlink, delete_symlink
 
@@ -49,6 +50,8 @@ class TestComprehensiveTheming(TestCase):
         dest_path = path(settings.COMPREHENSIVE_THEME_DIRS[0]) / tmp_theme
         create_symlink(themes_dir / tmp_theme, dest_path)
 
+        edxmako.paths.add_lookup('main', themes_dir, prepend=True)
+
         @with_comprehensive_theme(tmp_theme)
         def do_the_test(self):
             """A function to do the work so we can use the decorator."""
diff --git a/openedx/core/djangoapps/theming/helpers.py b/openedx/core/djangoapps/theming/helpers.py
index 24eee891a0..e9c30caff2 100644
--- a/openedx/core/djangoapps/theming/helpers.py
+++ b/openedx/core/djangoapps/theming/helpers.py
@@ -106,6 +106,8 @@ def get_template_path_with_theme(relative_path):
     Returns:
         (str): template path in current site's theme
     """
+    relative_path = os.path.normpath(relative_path)
+
     theme = get_current_theme()
 
     if not theme:
diff --git a/openedx/core/djangoapps/theming/tests/test_theme_style_overrides.py b/openedx/core/djangoapps/theming/tests/test_theme_style_overrides.py
index 72f81d9d9a..37445c2ae5 100644
--- a/openedx/core/djangoapps/theming/tests/test_theme_style_overrides.py
+++ b/openedx/core/djangoapps/theming/tests/test_theme_style_overrides.py
@@ -25,8 +25,7 @@ class TestComprehensiveThemeLMS(TestCase):
         # Clear the internal staticfiles caches, to get test isolation.
         staticfiles.finders.get_finder.cache_clear()
 
-    @override_settings(COMPREHENSIVE_THEME_DIRS=[settings.TEST_THEME.dirname()])
-    @with_comprehensive_theme(settings.TEST_THEME.basename())
+    @with_comprehensive_theme("test-theme")
     def test_footer(self):
         """
         Test that theme footer is used instead of default footer.
@@ -36,8 +35,7 @@ class TestComprehensiveThemeLMS(TestCase):
         # This string comes from header.html of test-theme
         self.assertContains(resp, "This is a footer for test-theme.")
 
-    @override_settings(COMPREHENSIVE_THEME_DIRS=[settings.TEST_THEME.dirname()])
-    @with_comprehensive_theme(settings.TEST_THEME.basename())
+    @with_comprehensive_theme("test-theme")
     def test_logo_image(self):
         """
         Test that theme logo is used instead of default logo.
@@ -61,8 +59,7 @@ class TestComprehensiveThemeCMS(TestCase):
         # Clear the internal staticfiles caches, to get test isolation.
         staticfiles.finders.get_finder.cache_clear()
 
-    @override_settings(COMPREHENSIVE_THEME_DIRS=[settings.TEST_THEME.dirname()])
-    @with_comprehensive_theme(settings.TEST_THEME.basename())
+    @with_comprehensive_theme("test-theme")
     def test_template_override(self):
         """
         Test that theme templates are used instead of default templates.
diff --git a/openedx/core/djangoapps/theming/tests/test_util.py b/openedx/core/djangoapps/theming/tests/test_util.py
index 8ead84bd62..7e0418ff00 100644
--- a/openedx/core/djangoapps/theming/tests/test_util.py
+++ b/openedx/core/djangoapps/theming/tests/test_util.py
@@ -32,9 +32,6 @@ def with_comprehensive_theme(theme_dir_name):
             site, __ = Site.objects.get_or_create(domain=domain, name=domain)
             site_theme, __ = SiteTheme.objects.get_or_create(site=site, theme_dir_name=theme_dir_name)
 
-            for _dir in settings.COMPREHENSIVE_THEME_DIRS:
-                edxmako.paths.add_lookup('main', _dir, prepend=True)
-
             with patch('openedx.core.djangoapps.theming.helpers.get_current_site_theme',
                        return_value=site_theme):
                 with patch('openedx.core.djangoapps.theming.helpers.get_current_site', return_value=site):
@@ -57,9 +54,6 @@ def with_comprehensive_theme_context(theme=None):
         site, __ = Site.objects.get_or_create(domain=domain, name=theme)
         site_theme, __ = SiteTheme.objects.get_or_create(site=site, theme_dir_name=theme)
 
-        for _dir in settings.COMPREHENSIVE_THEME_DIRS:
-            edxmako.paths.add_lookup('main', _dir, prepend=True)
-
         with patch('openedx.core.djangoapps.theming.helpers.get_current_site_theme',
                    return_value=site_theme):
             with patch('openedx.core.djangoapps.theming.helpers.get_current_site', return_value=site):