diff --git a/common/djangoapps/edxmako/paths.py b/common/djangoapps/edxmako/paths.py
index a29a68e8b3..518f8a530b 100644
--- a/common/djangoapps/edxmako/paths.py
+++ b/common/djangoapps/edxmako/paths.py
@@ -15,11 +15,14 @@ class DynamicTemplateLookup(TemplateLookup):
     A specialization of the standard mako `TemplateLookup` class which allows
     for adding directories progressively.
     """
-    def add_directory(self, directory):
+    def add_directory(self, directory, prepend=False):
         """
         Add a new directory to the template lookup path.
         """
-        self.directories.append(os.path.normpath(directory))
+        if prepend:
+            self.directories.insert(0, os.path.normpath(directory))
+        else:
+            self.directories.append(os.path.normpath(directory))
 
 
 def clear_lookups(namespace):
@@ -29,7 +32,7 @@ def clear_lookups(namespace):
     if namespace in LOOKUP:
         del LOOKUP[namespace]
 
-def add_lookup(namespace, directory, package=None):
+def add_lookup(namespace, directory, package=None, prepend=False):
     """
     Adds a new mako template lookup directory to the given namespace.
 
@@ -48,7 +51,7 @@ def add_lookup(namespace, directory, package=None):
         )
     if package:
         directory = pkg_resources.resource_filename(package, directory)
-    templates.add_directory(directory)
+    templates.add_directory(directory, prepend=prepend)
 
 
 def lookup_template(namespace, name):
diff --git a/lms/startup.py b/lms/startup.py
index 462fb3f8fd..ea4d27b167 100644
--- a/lms/startup.py
+++ b/lms/startup.py
@@ -52,8 +52,7 @@ def enable_theme():
 
     # Include the theme's templates in the template search paths
     settings.TEMPLATE_DIRS.insert(0, theme_root / 'templates')
-    settings.MAKO_TEMPLATES['main'].insert(0, theme_root / 'templates')
-    edxmako.startup.run()
+    edxmako.paths.add_lookup('main', theme_root / 'templates', prepend=True)
 
     # Namespace the theme's static files to 'themes/<theme_name>' to
     # avoid collisions with default edX static files
@@ -98,8 +97,7 @@ def enable_microsites():
     # if we have any valid microsites defined, let's wire in the Mako and STATIC_FILES search paths
     if microsite_config_dict:
         settings.TEMPLATE_DIRS.append(microsites_root)
-        settings.MAKO_TEMPLATES['main'].append(microsites_root)
-        edxmako.startup.run()
+        edxmako.paths.add_lookup('main', microsites_root)
 
         settings.STATICFILES_DIRS.insert(0, microsites_root)