diff --git a/openedx/core/djangoapps/content/block_structure/migrations/0004_blockstructuremodel_usagekeywithrun.py b/openedx/core/djangoapps/content/block_structure/migrations/0004_blockstructuremodel_usagekeywithrun.py
new file mode 100644
index 0000000000..670a8ae8bd
--- /dev/null
+++ b/openedx/core/djangoapps/content/block_structure/migrations/0004_blockstructuremodel_usagekeywithrun.py
@@ -0,0 +1,20 @@
+# -*- coding: utf-8 -*-
+from __future__ import unicode_literals
+
+from django.db import migrations, models
+import openedx.core.djangoapps.xmodule_django.models
+
+
+class Migration(migrations.Migration):
+
+    dependencies = [
+        ('block_structure', '0003_blockstructuremodel_storage'),
+    ]
+
+    operations = [
+        migrations.AlterField(
+            model_name='blockstructuremodel',
+            name='data_usage_key',
+            field=openedx.core.djangoapps.xmodule_django.models.UsageKeyWithRunField(unique=True, max_length=255, verbose_name='Identifier of the data being collected.'),
+        ),
+    ]
diff --git a/openedx/core/djangoapps/content/block_structure/models.py b/openedx/core/djangoapps/content/block_structure/models.py
index 3ae9b67273..b24010a4bb 100644
--- a/openedx/core/djangoapps/content/block_structure/models.py
+++ b/openedx/core/djangoapps/content/block_structure/models.py
@@ -11,7 +11,7 @@ from django.db import models, transaction
 from logging import getLogger
 
 from model_utils.models import TimeStampedModel
-from openedx.core.djangoapps.xmodule_django.models import UsageKeyField
+from openedx.core.djangoapps.xmodule_django.models import UsageKeyWithRunField
 from openedx.core.storage import get_storage
 
 from . import config
@@ -33,9 +33,12 @@ def _directory_name(data_usage_key):
     Returns the directory name for the given
     data_usage_key.
     """
+    # replace any '/' in the usage key so they aren't interpreted
+    # as folder separators.
+    encoded_usage_key = unicode(data_usage_key).replace('/', '_')
     return '{}{}'.format(
         settings.BLOCK_STRUCTURES_SETTINGS.get('DIRECTORY_PREFIX', ''),
-        unicode(data_usage_key),
+        encoded_usage_key,
     )
 
 
@@ -133,7 +136,7 @@ class BlockStructureModel(TimeStampedModel):
     class Meta(object):
         db_table = 'block_structure'
 
-    data_usage_key = UsageKeyField(
+    data_usage_key = UsageKeyWithRunField(
         u'Identifier of the data being collected.',
         blank=False,
         max_length=255,
diff --git a/openedx/core/djangoapps/content/block_structure/tests/test_models.py b/openedx/core/djangoapps/content/block_structure/tests/test_models.py
index a987ddc761..c455115167 100644
--- a/openedx/core/djangoapps/content/block_structure/tests/test_models.py
+++ b/openedx/core/djangoapps/content/block_structure/tests/test_models.py
@@ -14,7 +14,7 @@ from opaque_keys.edx.locator import CourseLocator, BlockUsageLocator
 
 from ..config import PRUNE_OLD_VERSIONS
 from ..exceptions import BlockStructureNotFound
-from ..models import BlockStructureModel, _storage_error_handling
+from ..models import BlockStructureModel, _directory_name, _storage_error_handling
 from .helpers import override_config_setting
 
 
@@ -44,7 +44,7 @@ class BlockStructureModelTestCase(TestCase):
             self.assertEqual(field_value, getattr(bsm, field_name))
 
         self.assertEqual(bsm.get_serialized_data(), expected_serialized_data)
-        self.assertIn(unicode(self.usage_key), bsm.data.name)
+        self.assertIn(_directory_name(self.usage_key), bsm.data.name)
 
     def _assert_file_count_equal(self, expected_count):
         """
@@ -160,3 +160,17 @@ class BlockStructureModelTestCase(TestCase):
         with self.assertRaises(expected_error_raised):
             with _storage_error_handling(bs_model, 'operation', is_read_operation):
                 raise error_raised_in_operation
+
+    @patch('openedx.core.djangoapps.content.block_structure.models.log')
+    def test_old_mongo_keys(self, mock_log):
+        self.course_key = CourseLocator('org2', 'course2', unicode(uuid4()), deprecated=True)
+        self.usage_key = BlockUsageLocator(course_key=self.course_key, block_type='course', block_id='course')
+        serialized_data = 'test data for old course'
+        self.params['data_usage_key'] = self.usage_key
+
+        with patch('xmodule.modulestore.mixed.MixedModuleStore.fill_in_run') as mock_fill_in_run:
+            mock_fill_in_run.return_value = self.usage_key.course_key
+            self._verify_update_or_create_call(serialized_data, mock_log, expect_created=True)
+            found_bsm = BlockStructureModel.get(self.usage_key)
+
+        self._assert_bsm_fields(found_bsm, serialized_data)
diff --git a/openedx/core/djangoapps/xmodule_django/models.py b/openedx/core/djangoapps/xmodule_django/models.py
index fe32953342..2987ca41e7 100644
--- a/openedx/core/djangoapps/xmodule_django/models.py
+++ b/openedx/core/djangoapps/xmodule_django/models.py
@@ -7,6 +7,8 @@ import logging
 from django.db import models
 from django.core.exceptions import ValidationError
 from opaque_keys.edx.keys import CourseKey, UsageKey, BlockTypeKey
+from xmodule.modulestore.django import modulestore
+
 
 log = logging.getLogger(__name__)
 
@@ -181,6 +183,18 @@ class UsageKeyField(OpaqueKeyField):
     KEY_CLASS = UsageKey
 
 
+class UsageKeyWithRunField(UsageKeyField):
+    """
+    Subclass of UsageKeyField that automatically fills in
+    missing `run` values, for old Mongo courses.
+    """
+    def to_python(self, value):
+        value = super(UsageKeyWithRunField, self).to_python(value)
+        if value is not None and value.run is None:
+            value = value.replace(course_key=modulestore().fill_in_run(value.course_key))
+        return value
+
+
 class LocationKeyField(UsageKeyField):
     """
     A django Field that stores a UsageKey object as a string.