diff --git a/lms/envs/common.py b/lms/envs/common.py
index ce08bf9666..61a3abab6d 100644
--- a/lms/envs/common.py
+++ b/lms/envs/common.py
@@ -260,12 +260,22 @@ STATICFILES_DIRS = [
     PROJECT_ROOT / "askbot" / "skins",
 ]
 if os.path.isdir(DATA_DIR):
+    # Add the full course repo if there is no static directory
     STATICFILES_DIRS += [
         # TODO (cpennington): When courses are stored in a database, this
         # should no longer be added to STATICFILES
         (course_dir, DATA_DIR / course_dir)
         for course_dir in os.listdir(DATA_DIR)
-        if os.path.isdir(DATA_DIR / course_dir)
+        if (os.path.isdir(DATA_DIR / course_dir) and
+            not os.path.isdir(DATA_DIR / course_dir / 'static'))
+    ]
+    # Otherwise, add only the static directory from the course dir
+    STATICFILES_DIRS += [
+        # TODO (cpennington): When courses are stored in a database, this
+        # should no longer be added to STATICFILES
+        (course_dir, DATA_DIR / course_dir / 'static')
+        for course_dir in os.listdir(DATA_DIR)
+        if (os.path.isdir(DATA_DIR / course_dir / 'static'))
     ]
 
 # Locale/Internationalization