diff --git a/config.py b/config.py
index 005ea4880..709129d84 100644
--- a/config.py
+++ b/config.py
@@ -23,7 +23,7 @@ CLIENT_WHITELIST = ['SERVER_HOSTNAME', 'PREFERRED_URL_SCHEME', 'MIXPANEL_KEY',
                     'CONTACT_INFO', 'AVATAR_KIND', 'LOCAL_OAUTH_HANDLER', 'DOCUMENTATION_LOCATION',
                     'DOCUMENTATION_METADATA', 'SETUP_COMPLETE', 'DEBUG', 'MARKETO_MUNCHKIN_ID',
                     'STATIC_SITE_BUCKET', 'RECAPTCHA_SITE_KEY', 'CHANNEL_COLORS',
-                    'TAG_EXPIRATION_OPTIONS']
+                    'TAG_EXPIRATION_OPTIONS', 'INTERNAL_OIDC_SERVICE_ID']
 
 
 def frontend_visible_config(config_dict):
diff --git a/data/users/__init__.py b/data/users/__init__.py
index 519947f8d..913823f91 100644
--- a/data/users/__init__.py
+++ b/data/users/__init__.py
@@ -10,6 +10,7 @@ from data.users.database import DatabaseUsers
 from data.users.externalldap import LDAPUsers
 from data.users.externaljwt import ExternalJWTAuthN
 from data.users.keystone import get_keystone_users
+from data.users.oidc import OIDCInternalAuth
 from util.security.aes import AESCipher
 
 logger = logging.getLogger(__name__)
@@ -24,6 +25,9 @@ def get_federated_service_name(authentication_type):
   if authentication_type == 'Keystone':
     return 'keystone'
 
+  if authentication_type == 'OIDC':
+    return 'oidc'
+
   raise Exception('Unknown auth type: %s' % authentication_type)
 
 
@@ -74,8 +78,15 @@ def get_users_handler(config, _, override_config_dir):
     keystone_admin_password = config.get('KEYSTONE_ADMIN_PASSWORD')
     keystone_admin_tenant = config.get('KEYSTONE_ADMIN_TENANT')
     return get_keystone_users(auth_version, auth_url, keystone_admin_username,
-                             keystone_admin_password, keystone_admin_tenant, timeout,
-                             requires_email=features.MAILING)
+                              keystone_admin_password, keystone_admin_tenant, timeout,
+                              requires_email=features.MAILING)
+
+  if authentication_type == 'OIDC':
+    if features.DIRECT_LOGIN:
+      raise Exception('Direct login feature must be disabled to use OIDC internal auth')
+
+    login_service = config.get('INTERNAL_OIDC_SERVICE_ID')
+    return OIDCInternalAuth(config, login_service, requires_email=features.MAILING)
 
   raise RuntimeError('Unknown authentication type: %s' % authentication_type)
 
@@ -160,6 +171,11 @@ class UserAuthentication(object):
     """
     return self.state.federated_service
 
+  @property
+  def supports_encrypted_credentials(self):
+    """ Returns whether this auth system supports using encrypted credentials. """
+    return self.state.supports_encrypted_credentials
+
   def query_users(self, query, limit=20):
     """ Performs a lookup against the user system for the specified query. The returned tuple
         will be of the form (results, federated_login_id, err_msg). If the method is unsupported,
diff --git a/data/users/database.py b/data/users/database.py
index ce04b3c9d..09a8ccf7f 100644
--- a/data/users/database.py
+++ b/data/users/database.py
@@ -9,6 +9,10 @@ class DatabaseUsers(object):
     """ Always assumed to be working. If the DB is broken, other checks will handle it. """
     return (True, None)
 
+  @property
+  def supports_encrypted_credentials(self):
+    return True
+
   def verify_credentials(self, username_or_email, password):
     """ Simply delegate to the model implementation. """
     result = model.user.verify_user(username_or_email, password)
diff --git a/data/users/federated.py b/data/users/federated.py
index 3c61a5837..944617a23 100644
--- a/data/users/federated.py
+++ b/data/users/federated.py
@@ -23,6 +23,10 @@ class FederatedUsers(object):
   def federated_service(self):
     return self._federated_service
 
+  @property
+  def supports_encrypted_credentials(self):
+    return True
+
   def get_user(self, username_or_email):
     """ Retrieves the user with the given username or email, returning a tuple containing
         a UserInformation (if success) and the error message (on failure).
diff --git a/data/users/oidc.py b/data/users/oidc.py
new file mode 100644
index 000000000..1014b513a
--- /dev/null
+++ b/data/users/oidc.py
@@ -0,0 +1,45 @@
+import logging
+
+from data.users.federated import FederatedUsers, UserInformation
+from oauth.loginmanager import OAuthLoginManager
+from oauth.oidc import PublicKeyLoadException
+from util.security.jwtutil import InvalidTokenError
+
+
+logger = logging.getLogger(__name__)
+
+
+class OIDCInternalAuth(FederatedUsers):
+  """ Handles authentication by delegating authentication to a signed OIDC JWT produced by the
+      configured OIDC service.
+  """
+  def __init__(self, config, login_service_id, requires_email):
+    super(OIDCInternalAuth, self).__init__('oidc', requires_email)
+    login_manager = OAuthLoginManager(config)
+    self.login_service = login_manager.get_service(login_service_id)
+    if self.login_service is None:
+      raise Exception('Unknown OIDC login service %s' % login_service_id)
+
+  @property
+  def supports_encrypted_credentials(self):
+    # Since the "password" is already a signed JWT.
+    return False
+
+  def get_user(self, username_or_email):
+    return (None, 'Cannot retrieve users for OIDC')
+
+  def query_users(self, query, limit=20):
+    return (None, 'Cannot query users for OIDC')
+
+  def verify_credentials(self, username_or_email, id_token):
+    try:
+      payload = self.login_service.decode_user_jwt(id_token)
+    except InvalidTokenError as ite:
+      logger.exception('Got invalid token error on OIDC decode: %s', ite.message)
+      return (None, 'Could not validate OIDC token')
+    except PublicKeyLoadException as pke:
+      logger.exception('Could not load public key during OIDC decode: %s', pke.message)
+      return (None, 'Could not validate OIDC token')
+
+    user_info = UserInformation(username=payload['sub'], id=payload['sub'], email=None)
+    return (user_info, None)
diff --git a/data/users/test/test_oidc.py b/data/users/test/test_oidc.py
new file mode 100644
index 000000000..5d7a8bfd4
--- /dev/null
+++ b/data/users/test/test_oidc.py
@@ -0,0 +1,19 @@
+from httmock import HTTMock
+
+from data.users.oidc import OIDCInternalAuth
+from oauth.test.test_oidc import (id_token, oidc_service, signing_key, jwks_handler,
+                                  discovery_handler, app_config, http_client,
+                                  discovery_content)
+
+def test_oidc_login(app_config, id_token, jwks_handler, discovery_handler):
+  internal_auth = OIDCInternalAuth(app_config, 'someoidc', False)
+  with HTTMock(jwks_handler, discovery_handler):
+    # Try a valid token.
+    (user, err) = internal_auth.verify_credentials('someusername', id_token)
+    assert err is None
+    assert user.username == 'cooluser'
+
+    # Try an invalid token.
+    (user, err) = internal_auth.verify_credentials('someusername', 'invalidtoken')
+    assert err is not None
+    assert user is None
diff --git a/endpoints/api/user.py b/endpoints/api/user.py
index 90ef38603..db705a806 100644
--- a/endpoints/api/user.py
+++ b/endpoints/api/user.py
@@ -513,6 +513,9 @@ class ClientKey(ApiResource):
   @validate_json_request('GenerateClientKey')
   def post(self):
     """  Return's the user's private client key. """
+    if not authentication.supports_encrypted_credentials:
+      raise NotFound()
+
     username = get_authenticated_user().username
     password = request.get_json()['password']
     (result, error_message) = authentication.confirm_existing_user(username, password)
@@ -728,7 +731,7 @@ class ExternalLoginInformation(ApiResource):
         'kind': {
           'type': 'string',
           'description': 'The kind of URL',
-          'enum': ['login', 'attach'],
+          'enum': ['login', 'attach', 'cli'],
         },
       },
     },
@@ -746,7 +749,7 @@ class ExternalLoginInformation(ApiResource):
 
     csrf_token = generate_csrf_token(OAUTH_CSRF_TOKEN_NAME)
     kind = request.get_json()['kind']
-    redirect_suffix = '/attach' if kind == 'attach' else ''
+    redirect_suffix = '/' if kind == 'login' else '/' + kind
 
     try:
       login_scopes = login_service.get_login_scopes()
diff --git a/endpoints/oauth/login.py b/endpoints/oauth/login.py
index 0a5e76618..c2080560c 100644
--- a/endpoints/oauth/login.py
+++ b/endpoints/oauth/login.py
@@ -250,6 +250,24 @@ def _register_service(login_service):
     auth_url = login_service.get_auth_url(app.config, '', csrf_token, login_scopes)
     return redirect(auth_url)
 
+  @require_session_login
+  @oauthlogin_csrf_protect
+  def cli_token_func():
+    # Check for a callback error.
+    error = request.args.get('error', None)
+    if error:
+      return _render_ologin_error(login_service.service_name(), error)
+
+    # Exchange the OAuth code for the ID token.
+    code = request.args.get('code')
+    try:
+      idtoken, _ = login_service.exchange_code_for_tokens(app.config, client, code, '/cli')
+    except OAuthLoginException as ole:
+      return _render_ologin_error(login_service.service_name(), ole.message)
+
+    user_obj = get_authenticated_user()
+    return redirect(url_for('web.user_view', path=user_obj.username, tab='settings',
+                            idtoken=idtoken))
 
   oauthlogin.add_url_rule('/%s/callback/captcha' % login_service.service_id(),
                           '%s_oauth_captcha' % login_service.service_id(),
@@ -266,6 +284,11 @@ def _register_service(login_service):
                           attach_func,
                           methods=['GET'])
 
+  oauthlogin.add_url_rule('/%s/callback/cli' % login_service.service_id(),
+                          '%s_oauth_cli' % login_service.service_id(),
+                          cli_token_func,
+                          methods=['GET'])
+
 # Register the routes for each of the login services.
 for current_service in oauth_login.services:
   _register_service(current_service)
diff --git a/initdb.py b/initdb.py
index c6b36e18e..2762751cf 100644
--- a/initdb.py
+++ b/initdb.py
@@ -267,6 +267,7 @@ def initialize_database():
   LoginService.create(name='jwtauthn')
   LoginService.create(name='keystone')
   LoginService.create(name='dex')
+  LoginService.create(name='oidc')
 
   BuildTriggerService.create(name='github')
   BuildTriggerService.create(name='custom-git')
diff --git a/oauth/loginmanager.py b/oauth/loginmanager.py
index 2504d661b..ea45890ea 100644
--- a/oauth/loginmanager.py
+++ b/oauth/loginmanager.py
@@ -1,7 +1,6 @@
 from oauth.services.github import GithubOAuthService
 from oauth.services.google import GoogleOAuthService
 from oauth.oidc import OIDCLoginService
-from data.users import UserAuthentication
 
 CUSTOM_LOGIN_SERVICES = {
   'GITHUB_LOGIN_CONFIG': GithubOAuthService,
diff --git a/oauth/oidc.py b/oauth/oidc.py
index 2b6e7cbc6..f5c9249a2 100644
--- a/oauth/oidc.py
+++ b/oauth/oidc.py
@@ -89,7 +89,7 @@ class OIDCLoginService(OAuthService):
       'OIDC': True,
     }
 
-  def exchange_code_for_login(self, app_config, http_client, code, redirect_suffix):
+  def exchange_code_for_tokens(self, app_config, http_client, code, redirect_suffix):
     # Exchange the code for the access token and id_token
     try:
       json_data = self.exchange_code(app_config, http_client, code,
@@ -109,9 +109,16 @@ class OIDCLoginService(OAuthService):
       logger.debug('Missing id_token in response: %s', json_data)
       raise OAuthLoginException('Missing `id_token` in OIDC response')
 
+    return id_token, access_token
+
+  def exchange_code_for_login(self, app_config, http_client, code, redirect_suffix):
+    # Exchange the code for the access token and id_token
+    id_token, access_token = self.exchange_code_for_tokens(app_config, http_client, code,
+                                                           redirect_suffix)
+
     # Decode the id_token.
     try:
-      decoded_id_token = self._decode_user_jwt(id_token)
+      decoded_id_token = self.decode_user_jwt(id_token)
     except InvalidTokenError as ite:
       logger.exception('Got invalid token error on OIDC decode: %s', ite.message)
       raise OAuthLoginException('Could not decode OIDC token')
@@ -181,7 +188,7 @@ class OIDCLoginService(OAuthService):
       logger.exception('Could not parse OIDC discovery for url: %s', discovery_url)
       raise DiscoveryFailureException("Could not parse OIDC discovery information")
 
-  def _decode_user_jwt(self, token):
+  def decode_user_jwt(self, token):
     """ Decodes the given JWT under the given provider and returns it. Raises an InvalidTokenError
         exception on an invalid token or a PublicKeyLoadException if the public key could not be
         loaded for decoding.
diff --git a/oauth/test/__init__.py b/oauth/test/__init__.py
new file mode 100644
index 000000000..e69de29bb
diff --git a/oauth/test/test_oidc.py b/oauth/test/test_oidc.py
index 98e914638..b1ea38a83 100644
--- a/oauth/test/test_oidc.py
+++ b/oauth/test/test_oidc.py
@@ -60,7 +60,7 @@ def app_config(http_client, mailing_feature):
     'SERVER_HOSTNAME': 'localhost',
     'FEATURE_MAILING': mailing_feature,
 
-    'SOMEOIDC_TEST_SERVICE': {
+    'SOMEOIDC_LOGIN_CONFIG': {
       'CLIENT_ID': 'foo',
       'CLIENT_SECRET': 'bar',
       'SERVICE_NAME': 'Some Cool Service',
@@ -74,7 +74,7 @@ def app_config(http_client, mailing_feature):
 
 @pytest.fixture()
 def oidc_service(app_config):
-  return OIDCLoginService(app_config, 'SOMEOIDC_TEST_SERVICE')
+  return OIDCLoginService(app_config, 'SOMEOIDC_LOGIN_CONFIG')
 
 @pytest.fixture()
 def discovery_content(userinfo_supported):
diff --git a/static/js/directives/ui/external-login-button.js b/static/js/directives/ui/external-login-button.js
index f2abfe6b8..41e6e0bca 100644
--- a/static/js/directives/ui/external-login-button.js
+++ b/static/js/directives/ui/external-login-button.js
@@ -21,7 +21,6 @@ angular.module('quay').directive('externalLoginButton', function () {
       $scope.startSignin = function() {
         $scope.signInStarted({'service': $scope.provider});
         ExternalLoginService.getLoginUrl($scope.provider, $scope.action || 'login', function(url) {
-
           // Save the redirect URL in a cookie so that we can redirect back after the service returns to us.
           var redirectURL = $scope.redirectUrl || window.location.toString();
           CookieService.putPermanent('quay.redirectAfterLoad', redirectURL);
diff --git a/static/js/pages/user-view.js b/static/js/pages/user-view.js
index c97a786b8..b66799879 100644
--- a/static/js/pages/user-view.js
+++ b/static/js/pages/user-view.js
@@ -13,6 +13,8 @@
   function UserViewCtrl($scope, $routeParams, $timeout, ApiService, UserService, UIService, AvatarService, Config, ExternalLoginService) {
     var username = $routeParams.username;
 
+    $scope.Config = Config;
+
     $scope.showAppsCounter = 0;
     $scope.showRobotsCounter = 0;
     $scope.showBillingCounter = 0;
@@ -23,7 +25,27 @@
     $scope.hasSingleSignin = ExternalLoginService.hasSingleSignin();
     $scope.context = {};
 
-    UserService.updateUserIn($scope);
+    $scope.oidcLoginProvider = null;
+
+    if (Config['INTERNAL_OIDC_SERVICE_ID']) {
+      ExternalLoginService.EXTERNAL_LOGINS.forEach(function(provider) {
+        if (provider.id == Config['INTERNAL_OIDC_SERVICE_ID']) {
+          $scope.oidcLoginProvider = provider;
+        }
+      });
+    }
+
+    UserService.updateUserIn($scope, function(user) {
+      if (user && user.username) {
+        if ($scope.oidcLoginProvider && $routeParams['idtoken']) {
+          $scope.context.idTokenCredentials = {
+            'username': UserService.getCLIUsername(),
+            'password': $routeParams['idtoken'],
+            'namespace': UserService.currentUser().username
+          };
+        }
+      }
+    });
 
     var loadRepositories = function() {
       var options = {
diff --git a/static/partials/user-view.html b/static/partials/user-view.html
index e9ea15f99..3a2eb5549 100644
--- a/static/partials/user-view.html
+++ b/static/partials/user-view.html
@@ -70,8 +70,25 @@
 
         <!-- Settings -->
         <cor-tab-pane id="settings">
+          <!-- OIDC Token -->
+          <div class="settings-section" ng-if="Config.AUTHENTICATION_TYPE == 'OIDC'">
+            <h3>Docker CLI Token</h3>
+            <div>
+              A generated token is <strong>required</strong> to login via the Docker CLI.
+            </div>
+
+            <table class="co-list-table" style="margin-top: 10px;">
+              <tr>
+                <td>CLI Token:</td>
+                <td>
+                  <span class="external-login-button" is-link="true" action="cli" provider="oidcLoginProvider"></span>
+                </td>
+              </tr>
+            </table>
+          </div>
+
           <!-- Encrypted Password -->
-          <div class="settings-section">
+          <div class="settings-section" ng-if="Config.AUTHENTICATION_TYPE != 'OIDC'">
             <h3>Docker CLI Password</h3>
             <div ng-if="!Features.REQUIRE_ENCRYPTED_BASIC_AUTH">
               The Docker CLI stores passwords entered on the command line in <strong>plaintext</strong>. It is therefore highly recommended to generate an an encrypted version of your password to use for <code>docker login</code>.
@@ -185,4 +202,7 @@
 
   <!-- Credentials for encrypted passwords -->
   <div class="credentials-dialog" credentials="context.encryptedPasswordCredentials" secret-title="Encrypted Password" entity-title="encrypted password" entity-icon="fa-key">
+
+  <!-- Credentials for ID token -->
+  <div class="credentials-dialog" credentials="context.idTokenCredentials" secret-title="CLI Token" entity-title="Docker CLI token" entity-icon="fa-key">
 </div>