diff --git a/data/registry_model/shared.py b/data/registry_model/shared.py
index 8b62d86fd..ebed550af 100644
--- a/data/registry_model/shared.py
+++ b/data/registry_model/shared.py
@@ -12,6 +12,7 @@ from data.registry_model.datatype import FromDictionaryException
 from data.registry_model.datatypes import (RepositoryReference, Blob, TorrentInfo, BlobUpload,
                                            LegacyImage, ManifestLayer, DerivedImage)
 from image.docker.schema1 import ManifestException, DockerSchema1ManifestBuilder
+from image.docker.schema2 import EMPTY_LAYER_BLOB_DIGEST
 
 logger = logging.getLogger(__name__)
 
@@ -344,14 +345,21 @@ class SharedModel:
         working towards the leaf, including the associated Blob and its placements (if specified).
         Returns None if the manifest could not be parsed and validated.
     """
+    retriever = RepositoryContentRetriever(repo_id, storage)
+    requires_empty_blob = parsed.get_requires_empty_layer_blob(retriever)
+
     storage_map = {}
-    if parsed.local_blob_digests:
+    blob_digests = list(parsed.local_blob_digests)
+    if requires_empty_blob:
+      blob_digests.append(EMPTY_LAYER_BLOB_DIGEST)
+
+    if blob_digests:
       blob_query = model.storage.lookup_repo_storages_by_content_checksum(repo_id,
-                                                                          parsed.local_blob_digests,
+                                                                          blob_digests,
                                                                           by_manifest=by_manifest)
       storage_map = {blob.content_checksum: blob for blob in blob_query}
 
-    retriever = RepositoryContentRetriever(repo_id, storage)
+
     layers = parsed.get_layers(retriever)
     if layers is None:
       logger.error('Could not load layers for manifest `%s`', parsed.digest)
diff --git a/endpoints/api/manifest.py b/endpoints/api/manifest.py
index 3183796d5..32012d4cf 100644
--- a/endpoints/api/manifest.py
+++ b/endpoints/api/manifest.py
@@ -1,5 +1,6 @@
 """ Manage the manifests of a repository. """
 import json
+import logging
 
 from flask import request
 
@@ -20,6 +21,9 @@ BASE_MANIFEST_ROUTE = '/v1/repository/<apirepopath:repository>/manifest/<regex("
 MANIFEST_DIGEST_ROUTE = BASE_MANIFEST_ROUTE.format(digest_tools.DIGEST_PATTERN)
 ALLOWED_LABEL_MEDIA_TYPES = ['text/plain', 'application/json']
 
+
+logger = logging.getLogger(__name__)
+
 def _label_dict(label):
   return {
     'id': label.uuid,
@@ -31,10 +35,12 @@ def _label_dict(label):
 
 
 def _layer_dict(manifest_layer, index):
+  # NOTE: The `command` in the layer is either a JSON string of an array (schema 1) or
+  # a single string (schema 2). The block below normalizes it to have the same format.
   try:
     command = json.loads(manifest_layer.command)
   except (TypeError, ValueError):
-    command = []
+    command = [manifest_layer.command]
 
   return {
     'index': index,
@@ -53,6 +59,10 @@ def _manifest_dict(manifest):
     image = image_dict(manifest.legacy_image, with_history=True)
 
   layers = registry_model.list_manifest_layers(manifest, storage)
+  if layers is None and not manifest.is_manifest_list:
+    logger.debug('Missing layers for manifest `%s`', manifest.digest)
+    abort(404)
+
   return {
     'digest': manifest.digest,
     'is_manifest_list': manifest.is_manifest_list,