diff --git a/tests/test_updater.py b/tests/test_updater.py
index 3967ec07..d00f2741 100644
--- a/tests/test_updater.py
+++ b/tests/test_updater.py
@@ -224,6 +224,9 @@ def test_1__init__exceptions(self):
     # directory.
     tuf.settings.repositories_directory = self.client_directory
 
+    # Test: repository does not exist
+    self.assertRaises(tuf.exceptions.MissingLocalRepositoryError, updater.Updater,
+                      'test_non_existing_repository', self.repository_mirrors)
 
     # Test: empty client repository (i.e., no metadata directory).
     metadata_backup = self.client_metadata + '.backup'
diff --git a/tuf/client/updater.py b/tuf/client/updater.py
index 4e621124..0d96322a 100755
--- a/tuf/client/updater.py
+++ b/tuf/client/updater.py
@@ -727,6 +727,12 @@ def __init__(self, repository_name, repository_mirrors):
     # Set the path for the current set of metadata files.
     repositories_directory = tuf.settings.repositories_directory
     repository_directory = os.path.join(repositories_directory, self.repository_name)
+
+    # raise MissingLocalRepository if the repo does not exist at all.
+    if not os.path.exists(repository_directory):
+      raise tuf.exceptions.MissingLocalRepositoryError('Local repository ' +
+        repr(repository_directory) + ' does not exist.')
+
     current_path = os.path.join(repository_directory, 'metadata', 'current')
 
     # Ensure the current path is valid/exists before saving it.
diff --git a/tuf/exceptions.py b/tuf/exceptions.py
index bd75b312..177e7a29 100755
--- a/tuf/exceptions.py
+++ b/tuf/exceptions.py
@@ -115,6 +115,10 @@ class RepositoryError(Error):
   """Indicate an error with a repository's state, such as a missing file."""
 
 
+class MissingLocalRepositoryError(RepositoryError):
+  """Raised when a local repository could not be found."""
+
+
 class InsufficientKeysError(Error):
   """Indicate that metadata role lacks a threshold of pubic or private keys."""