diff --git a/common/djangoapps/microsite_configuration/apps.py b/common/djangoapps/microsite_configuration/apps.py
new file mode 100644
index 0000000000..6233628385
--- /dev/null
+++ b/common/djangoapps/microsite_configuration/apps.py
@@ -0,0 +1,15 @@
+
+import logging
+from django.apps import AppConfig
+from .microsite import enable_microsites
+
+log = logging.getLogger(__name__)
+
+
+class MicrositeConfigurationConfig(AppConfig):
+    name = 'microsite_configuration'
+    verbose_name = "Microsite Configuration"
+
+    def ready(self):
+        # Mako requires the directories to be added after the django setup.
+        enable_microsites(log)
diff --git a/lms/envs/common.py b/lms/envs/common.py
index ae9079993d..4fb74b49c0 100644
--- a/lms/envs/common.py
+++ b/lms/envs/common.py
@@ -557,6 +557,8 @@ def _make_main_mako_templates(settings):
         for theme in get_themes_unchecked(themes_dirs, PROJECT_ROOT):
             if theme.themes_base_dir not in settings.MAIN_MAKO_TEMPLATES_BASE:
                 settings.MAIN_MAKO_TEMPLATES_BASE.insert(0, theme.themes_base_dir)
+    if settings.FEATURES.get('USE_MICROSITES', False) and getattr(settings, "MICROSITE_CONFIGURATION", False):
+        settings.MAIN_MAKO_TEMPLATES_BASE.insert(0, settings.MICROSITE_ROOT_DIR)
     return settings.MAIN_MAKO_TEMPLATES_BASE
 MAKO_TEMPLATES['main'] = _make_main_mako_templates
 derived_dict_entry('MAKO_TEMPLATES', 'main')
@@ -620,6 +622,18 @@ TEMPLATES = [
     }
 ]
 DEFAULT_TEMPLATE_ENGINE = TEMPLATES[0]
+DEFAULT_TEMPLATE_ENGINE_DIRS = DEFAULT_TEMPLATE_ENGINE['DIRS'][:]
+
+
+def _add_microsite_dirs_to_default_template_engine(settings):
+    """
+    Derives the final DEFAULT_TEMPLATE_ENGINE['DIRS'] setting from other settings.
+    """
+    if settings.FEATURES.get('USE_MICROSITES', False) and getattr(settings, "MICROSITE_CONFIGURATION", False):
+        DEFAULT_TEMPLATE_ENGINE_DIRS.append(settings.MICROSITE_ROOT_DIR)
+    return DEFAULT_TEMPLATE_ENGINE_DIRS
+DEFAULT_TEMPLATE_ENGINE['DIRS'] = _add_microsite_dirs_to_default_template_engine
+derived_dict_entry('DEFAULT_TEMPLATE_ENGINE', 'DIRS')
 
 ###############################################################################################
 
@@ -2176,7 +2190,7 @@ INSTALLED_APPS = [
     'openedx.core.djangoapps.dark_lang',
 
     # Microsite configuration
-    'microsite_configuration',
+    'microsite_configuration.apps.MicrositeConfigurationConfig',
 
     # RSS Proxy
     'rss_proxy',
diff --git a/lms/startup.py b/lms/startup.py
index 83055939c9..0afc7f782b 100644
--- a/lms/startup.py
+++ b/lms/startup.py
@@ -21,8 +21,6 @@ import lms_xblock.runtime
 
 from startup_configurations.validate_config import validate_lms_config
 
-from microsite_configuration import microsite
-
 log = logging.getLogger(__name__)
 
 
@@ -35,20 +33,12 @@ def run():
     """
     django_db_models_options.patch()
 
-    # We currently use 2 template rendering engines, mako and django_templates,
-    # and one of them (django templates), requires the directories be added
-    # before the django.setup().
-    microsite.enable_microsites_pre_startup(log)
-
     django.setup()
 
     autostartup()
 
     add_mimetypes()
 
-    # Mako requires the directories to be added after the django setup.
-    microsite.enable_microsites(log)
-
     # In order to allow modules to use a handler url, we need to
     # monkey-patch the x_module library.
     # TODO: Remove this code when Runtimes are no longer created by modulestores
diff --git a/lms/tests.py b/lms/tests.py
index cddcc181d9..bab5c7df1e 100644
--- a/lms/tests.py
+++ b/lms/tests.py
@@ -1,5 +1,6 @@
 """Tests for the lms module itself."""
 
+import logging
 import mimetypes
 
 from django.core.urlresolvers import reverse
@@ -7,11 +8,13 @@ from django.test import TestCase
 from mock import patch
 
 from edxmako import LOOKUP, add_lookup
-from lms import startup
+from microsite_configuration import microsite
 from openedx.features.course_experience import course_home_url_name
 from xmodule.modulestore.tests.django_utils import ModuleStoreTestCase
 from xmodule.modulestore.tests.factories import CourseFactory
 
+log = logging.getLogger(__name__)
+
 
 class LmsModuleTests(TestCase):
     """
@@ -38,7 +41,7 @@ class TemplateLookupTests(TestCase):
         self.assertEqual(len([directory for directory in directories if 'external_module' in directory]), 1)
 
         # This should not clear the directories list
-        startup.enable_microsites()
+        microsite.enable_microsites(log)
         directories = LOOKUP['main'].directories
         self.assertEqual(len([directory for directory in directories if 'external_module' in directory]), 1)