diff --git a/endpoints/api/__init__.py b/endpoints/api/__init__.py
index d9c3d0fb0..6a9369d8d 100644
--- a/endpoints/api/__init__.py
+++ b/endpoints/api/__init__.py
@@ -32,7 +32,7 @@ logger = logging.getLogger(__name__)
 api_bp = Blueprint('api', __name__)
 api = Api()
 api.init_app(api_bp)
-api.decorators = [csrf_protect,
+api.decorators = [csrf_protect(),
                   crossdomain(origin='*', headers=['Authorization', 'Content-Type']),
                   process_oauth, time_decorator(api_bp.name, metric_queue)]
 
diff --git a/endpoints/api/user.py b/endpoints/api/user.py
index 5457132e8..114ac7277 100644
--- a/endpoints/api/user.py
+++ b/endpoints/api/user.py
@@ -26,6 +26,7 @@ from endpoints.api import (ApiResource, nickname, resource, validate_json_reques
 from endpoints.exception import NotFound, InvalidToken
 from endpoints.api.subscribe import subscribe
 from endpoints.common import common_login
+from endpoints.csrf import generate_csrf_token, OAUTH_CSRF_TOKEN_NAME
 from endpoints.decorators import anon_allowed
 from util.useremails import (send_confirmation_email, send_recovery_email, send_change_email,
                              send_password_changed, send_org_recovery_email)
@@ -673,6 +674,15 @@ class Signout(ApiResource):
     return {'success': True}
 
 
+@resource('/v1/externaltoken')
+@internal_only
+class GenerateExternalToken(ApiResource):
+  """ Resource for generating a token for external login. """
+  @nickname('generateExternalLoginToken')
+  def post(self):
+    """ Generates a CSRF token explicitly for OIDC/OAuth-associated login. """
+    return {'token': generate_csrf_token(OAUTH_CSRF_TOKEN_NAME)}
+
 
 @resource('/v1/detachexternal/<servicename>')
 @show_if(features.DIRECT_LOGIN)
diff --git a/endpoints/csrf.py b/endpoints/csrf.py
index 39a0d636b..b2dbfcff1 100644
--- a/endpoints/csrf.py
+++ b/endpoints/csrf.py
@@ -1,9 +1,10 @@
 import logging
 import os
 import base64
+import hmac
 
-from flask import session, request
 from functools import wraps
+from flask import session, request
 
 from app import app
 from auth.auth_context import get_validated_oauth_token
@@ -12,31 +13,47 @@ from util.http import abort
 
 logger = logging.getLogger(__name__)
 
+OAUTH_CSRF_TOKEN_NAME = '_oauth_csrf_token'
+_QUAY_CSRF_TOKEN_NAME = '_csrf_token'
 
-def generate_csrf_token():
-  if '_csrf_token' not in session:
-    session['_csrf_token'] = base64.b64encode(os.urandom(48))
+def generate_csrf_token(session_token_name=_QUAY_CSRF_TOKEN_NAME):
+  """ If not present in the session, generates a new CSRF token with the given name
+      and places it into the session. Returns the generated token.
+  """
+  if session_token_name not in session:
+    session[session_token_name] = base64.b64encode(os.urandom(48))
 
-  return session['_csrf_token']
+  return session[session_token_name]
 
-def verify_csrf():
-  token = session.get('_csrf_token', None)
-  found_token = request.values.get('_csrf_token', None)
 
-  if not token or token != found_token:
-    msg = 'CSRF Failure. Session token was %s and request token was %s'
-    logger.error(msg, token, found_token)
+def verify_csrf(session_token_name=_QUAY_CSRF_TOKEN_NAME,
+                request_token_name=_QUAY_CSRF_TOKEN_NAME):
+  """ Verifies that the CSRF token with the given name is found in the session and
+      that the matching token is found in the request args or values.
+  """
+  token = str(session.get(session_token_name, ''))
+  found_token = str(request.values.get(request_token_name, ''))
+
+  if not token or not found_token or not hmac.compare_digest(token, found_token):
+    msg = 'CSRF Failure. Session token (%s) was %s and request token (%s) was %s'
+    logger.error(msg, session_token_name, token, request_token_name, found_token)
     abort(403, message='CSRF token was invalid or missing.')
 
-def csrf_protect(func):
-  @wraps(func)
-  def wrapper(*args, **kwargs):
-    oauth_token = get_validated_oauth_token()
-    if oauth_token is None and request.method != "GET" and request.method != "HEAD":
-      verify_csrf()
 
-    return func(*args, **kwargs)
-  return wrapper
+def csrf_protect(session_token_name=_QUAY_CSRF_TOKEN_NAME,
+                 request_token_name=_QUAY_CSRF_TOKEN_NAME,
+                 all_methods=False):
+  def inner(func):
+    @wraps(func)
+    def wrapper(*args, **kwargs):
+      oauth_token = get_validated_oauth_token()
+      if oauth_token is None:
+        if all_methods or (request.method != "GET" and request.method != "HEAD"):
+          verify_csrf(session_token_name, request_token_name)
+
+      return func(*args, **kwargs)
+    return wrapper
+  return inner
 
 
 app.jinja_env.globals['csrf_token'] = generate_csrf_token
diff --git a/endpoints/oauthlogin.py b/endpoints/oauthlogin.py
index a750f5519..17cb6da20 100644
--- a/endpoints/oauthlogin.py
+++ b/endpoints/oauthlogin.py
@@ -12,6 +12,7 @@ from auth.process import require_session_login
 from data import model
 from endpoints.common import common_login, route_show_if
 from endpoints.web import index
+from endpoints.csrf import csrf_protect, OAUTH_CSRF_TOKEN_NAME
 from util.security.jwtutil import decode, InvalidTokenError
 from util.validation import generate_valid_usernames
 
@@ -19,6 +20,7 @@ logger = logging.getLogger(__name__)
 client = app.config['HTTPCLIENT']
 oauthlogin = Blueprint('oauthlogin', __name__)
 
+oauthlogin_csrf_protect = csrf_protect(OAUTH_CSRF_TOKEN_NAME, 'state', all_methods=True)
 
 def render_ologin_error(service_name, error_message=None, register_redirect=False):
   user_creation = bool(features.USER_CREATION and features.DIRECT_LOGIN)
@@ -30,7 +32,11 @@ def render_ologin_error(service_name, error_message=None, register_redirect=Fals
     'user_creation': user_creation,
     'register_redirect': register_redirect,
   }
-  return index('', error_info=error_info)
+
+  resp = index('', error_info=error_info)
+  resp.status_code = 400
+  return resp
+
 
 def get_user(service, token):
   token_param = {
@@ -44,7 +50,7 @@ def get_user(service, token):
   return got_user.json()
 
 
-def conduct_oauth_login(service, user_id, username, email, metadata={}):
+def conduct_oauth_login(service, user_id, username, email, metadata=None):
   service_name = service.service_name()
   to_login = model.user.verify_federated_login(service_name.lower(), user_id)
   if not to_login:
@@ -66,17 +72,12 @@ def conduct_oauth_login(service, user_id, username, email, metadata={}):
       prompts = model.user.get_default_user_prompts(features)
       to_login = model.user.create_federated_user(new_username, email, service_name.lower(),
                                                   user_id, set_password_notification=True,
-                                                  metadata=metadata,
+                                                  metadata=metadata or {},
                                                   prompts=prompts)
 
       # Success, tell analytics
       analytics.track(to_login.username, 'register', {'service': service_name.lower()})
 
-      state = request.args.get('state', None)
-      if state:
-        logger.debug('Aliasing with state: %s', state)
-        analytics.alias(to_login.username, state)
-
     except model.InvalidEmailAddressException:
       message = "The e-mail address %s is already associated " % (email, )
       message = message + "with an existing %s account." % (app.config['REGISTRY_TITLE_SHORT'], )
@@ -96,6 +97,7 @@ def conduct_oauth_login(service, user_id, username, email, metadata={}):
 
   return render_ologin_error(service_name)
 
+
 def get_email_username(user_data):
   username = user_data['email']
   at = username.find('@')
@@ -107,6 +109,7 @@ def get_email_username(user_data):
 
 @oauthlogin.route('/google/callback', methods=['GET'])
 @route_show_if(features.GOOGLE_LOGIN)
+@oauthlogin_csrf_protect
 def google_oauth_callback():
   error = request.args.get('error', None)
   if error:
@@ -114,6 +117,9 @@ def google_oauth_callback():
 
   code = request.args.get('code')
   token = google_login.exchange_code_for_token(app.config, client, code, form_encode=True)
+  if token is None:
+    return render_ologin_error('Google')
+
   user_data = get_user(google_login, token)
   if not user_data or not user_data.get('id', None) or not user_data.get('email', None):
     return render_ologin_error('Google')
@@ -136,6 +142,7 @@ def google_oauth_callback():
 
 @oauthlogin.route('/github/callback', methods=['GET'])
 @route_show_if(features.GITHUB_LOGIN)
+@oauthlogin_csrf_protect
 def github_oauth_callback():
   error = request.args.get('error', None)
   if error:
@@ -144,10 +151,12 @@ def github_oauth_callback():
   # Exchange the OAuth code.
   code = request.args.get('code')
   token = github_login.exchange_code_for_token(app.config, client, code)
+  if token is None:
+    return render_ologin_error('GitHub')
 
   # Retrieve the user's information.
   user_data = get_user(github_login, token)
-  if not user_data or not 'login' in user_data:
+  if not user_data or 'login' not in user_data:
     return render_ologin_error('GitHub')
 
   username = user_data['login']
@@ -167,7 +176,8 @@ def github_oauth_callback():
                           headers={'Accept': 'application/vnd.github.moondragon+json'})
 
     organizations = set([org.get('login').lower() for org in get_orgs.json()])
-    if not (organizations & set(github_login.allowed_organizations())):
+    matching_organizations = organizations & set(github_login.allowed_organizations())
+    if not matching_organizations:
       err = """You are not a member of an allowed GitHub organization.
                Please contact your system administrator if you believe this is in error."""
       return render_ologin_error('GitHub', err)
@@ -175,6 +185,8 @@ def github_oauth_callback():
   # Find the e-mail address for the user: we will accept any email, but we prefer the primary
   get_email = client.get(github_login.email_endpoint(), params=token_param,
                          headers=v3_media_type)
+  if get_email.status_code / 100 != 2:
+    return render_ologin_error('GitHub')
 
   found_email = None
   for user_email in get_email.json():
@@ -199,10 +211,13 @@ def github_oauth_callback():
 @oauthlogin.route('/google/callback/attach', methods=['GET'])
 @route_show_if(features.GOOGLE_LOGIN)
 @require_session_login
+@oauthlogin_csrf_protect
 def google_oauth_attach():
   code = request.args.get('code')
   token = google_login.exchange_code_for_token(app.config, client, code,
                                                redirect_suffix='/attach', form_encode=True)
+  if token is None:
+    return render_ologin_error('Google')
 
   user_data = get_user(google_login, token)
   if not user_data or not user_data.get('id', None):
@@ -236,9 +251,13 @@ def google_oauth_attach():
 @oauthlogin.route('/github/callback/attach', methods=['GET'])
 @route_show_if(features.GITHUB_LOGIN)
 @require_session_login
+@oauthlogin_csrf_protect
 def github_oauth_attach():
   code = request.args.get('code')
   token = github_login.exchange_code_for_token(app.config, client, code)
+  if token is None:
+    return render_ologin_error('GitHub')
+
   user_data = get_user(github_login, token)
   if not user_data:
     return render_ologin_error('GitHub')
@@ -276,6 +295,7 @@ def decode_user_jwt(token, oidc_provider):
 
 @oauthlogin.route('/dex/callback', methods=['GET', 'POST'])
 @route_show_if(features.DEX_LOGIN)
+@oauthlogin_csrf_protect
 def dex_oauth_callback():
   error = request.values.get('error', None)
   if error:
@@ -287,6 +307,8 @@ def dex_oauth_callback():
 
   token = dex_login.exchange_code_for_token(app.config, client, code, client_auth=True,
                                             form_encode=True)
+  if token is None:
+    return render_ologin_error(dex_login.public_title)
 
   try:
     payload = decode_user_jwt(token, dex_login)
@@ -318,11 +340,12 @@ def dex_oauth_callback():
 @oauthlogin.route('/dex/callback/attach', methods=['GET', 'POST'])
 @route_show_if(features.DEX_LOGIN)
 @require_session_login
+@oauthlogin_csrf_protect
 def dex_oauth_attach():
   code = request.args.get('code')
   token = dex_login.exchange_code_for_token(app.config, client, code, redirect_suffix='/attach',
                                             client_auth=True, form_encode=True)
-  if not token:
+  if token is None:
     return render_ologin_error(dex_login.public_title)
 
   try:
@@ -346,4 +369,3 @@ def dex_oauth_attach():
     return render_ologin_error(dex_login.public_title, err)
 
   return redirect(url_for('web.user_view', path=user_obj.username, tab='external'))
-
diff --git a/endpoints/web.py b/endpoints/web.py
index 03fec46f6..f3a6f7ce7 100644
--- a/endpoints/web.py
+++ b/endpoints/web.py
@@ -494,7 +494,7 @@ def oauth_local_handler():
 
 
 @web.route('/oauth/denyapp', methods=['POST'])
-@csrf_protect
+@csrf_protect()
 def deny_application():
   if not current_user.is_authenticated:
     abort(401)
diff --git a/static/js/app.js b/static/js/app.js
index bdffb9451..ba49e6181 100644
--- a/static/js/app.js
+++ b/static/js/app.js
@@ -215,7 +215,8 @@ quayApp.config(['$routeProvider', '$locationProvider', 'pages', function($routeP
     // 404/403
     .route('/:catchall', 'error-view')
     .route('/:catch/:all', 'error-view')
-    .route('/:catch/:all/:things', 'error-view');
+    .route('/:catch/:all/:things', 'error-view')
+    .route('/:catch/:all/:things/:here', 'error-view');
 }]);
 
 // Configure compile provider to add additional URL prefixes to the sanitization list. We use
diff --git a/static/js/directives/ui/external-login-button.js b/static/js/directives/ui/external-login-button.js
index 509b2b489..f8ec07e53 100644
--- a/static/js/directives/ui/external-login-button.js
+++ b/static/js/directives/ui/external-login-button.js
@@ -21,19 +21,21 @@ angular.module('quay').directive('externalLoginButton', function () {
 
       $scope.startSignin = function() {
         $scope.signInStarted({'service': $scope.provider});
+        ApiService.generateExternalLoginToken().then(function(data) {
+          var url = ExternalLoginService.getLoginUrl($scope.provider, $scope.action || 'login');
+          url = url + '&state=' + encodeURIComponent(data['token']);
 
-        var url = ExternalLoginService.getLoginUrl($scope.provider, $scope.action || 'login');
+          // 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);
 
-        // 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);
-
-        // Needed to ensure that UI work done by the started callback is finished before the location
-        // changes.
-        $scope.signingIn = true;
-        $timeout(function() {
-          document.location = url;
-        }, 250);
+          // Needed to ensure that UI work done by the started callback is finished before the location
+          // changes.
+          $scope.signingIn = true;
+          $timeout(function() {
+            document.location = url;
+          }, 250);
+        }, ApiService.errorDisplay('Could not perform sign in'));
       };
     }
   };
diff --git a/static/js/services/external-login-service.js b/static/js/services/external-login-service.js
index 91197e7b4..7d6061df6 100644
--- a/static/js/services/external-login-service.js
+++ b/static/js/services/external-login-service.js
@@ -9,14 +9,6 @@ angular.module('quay').factory('ExternalLoginService', ['KeyService', 'Features'
     var serviceInfo = externalLoginService.getProvider(service);
     if (!serviceInfo) { return ''; }
 
-    var stateClause = '';
-
-    if (Config.MIXPANEL_KEY && window.mixpanel) {
-      if (mixpanel.get_distinct_id !== undefined) {
-        stateClause = "&state=" + encodeURIComponent(mixpanel.get_distinct_id());
-      }
-    }
-
     var loginUrl = KeyService.getConfiguration(serviceInfo.key, 'AUTHORIZE_ENDPOINT');
     var clientId = KeyService.getConfiguration(serviceInfo.key, 'CLIENT_ID');
 
@@ -28,8 +20,7 @@ angular.module('quay').factory('ExternalLoginService', ['KeyService', 'Features'
     }
 
     var url = loginUrl + 'client_id=' + clientId + '&scope=' + scope + '&redirect_uri=' +
-              redirectUri + stateClause;
-
+              redirectUri;
     return url;
   };
 
diff --git a/test/test_api_usage.py b/test/test_api_usage.py
index 1bfb8f9dc..f89003972 100644
--- a/test/test_api_usage.py
+++ b/test/test_api_usage.py
@@ -124,9 +124,11 @@ class ApiTestCase(unittest.TestCase):
     query[CSRF_TOKEN_KEY] = CSRF_TOKEN
     return urlunparse(list(parts[0:4]) + [urlencode(query)] + list(parts[5:]))
 
-  def url_for(self, resource_name, params={}):
+  def url_for(self, resource_name, params=None, skip_csrf=False):
+    params = params or {}
     url = api.url_for(resource_name, **params)
-    url = ApiTestCase._add_csrf(url)
+    if not skip_csrf:
+      url = ApiTestCase._add_csrf(url)
     return url
 
   def setUp(self):
@@ -211,8 +213,8 @@ class ApiTestCase(unittest.TestCase):
     return parsed
 
   def putJsonResponse(self, resource_name, params={}, data={},
-                      expected_code=200):
-    rv = self.app.put(self.url_for(resource_name, params),
+                      expected_code=200, skip_csrf=False):
+    rv = self.app.put(self.url_for(resource_name, params, skip_csrf),
                       data=py_json.dumps(data),
                       headers={"Content-Type": "application/json"})
 
@@ -246,15 +248,35 @@ class TestCSRFFailure(ApiTestCase):
     self.login(READ_ACCESS_USER)
 
     # Make sure a simple post call succeeds.
-    self.putJsonResponse(User,
-                         data=dict(password='newpasswordiscool'))
+    self.putJsonResponse(User, data=dict(password='newpasswordiscool'))
 
     # Change the session's CSRF token.
     self.setCsrfToken('someinvalidtoken')
 
     # Verify that the call now fails.
-    self.putJsonResponse(User,
-                         data=dict(password='newpasswordiscool'),
+    self.putJsonResponse(User, data=dict(password='newpasswordiscool'), expected_code=403)
+
+  def test_csrf_failure_empty_token(self):
+    self.login(READ_ACCESS_USER)
+
+    # Change the session's CSRF token to be empty.
+    self.setCsrfToken('')
+
+    # Verify that the call now fails.
+    self.putJsonResponse(User, data=dict(password='newpasswordiscool'), expected_code=403)
+
+  def test_csrf_failure_missing_token(self):
+    self.login(READ_ACCESS_USER)
+
+    # Make sure a simple post call without a token at all fails.
+    self.putJsonResponse(User, data=dict(password='newpasswordiscool'), skip_csrf=True,
+                         expected_code=403)
+
+    # Change the session's CSRF token to be empty.
+    self.setCsrfToken('')
+
+    # Verify that the call still fails.
+    self.putJsonResponse(User, data=dict(password='newpasswordiscool'), skip_csrf=True,
                          expected_code=403)
 
 
diff --git a/test/test_endpoints.py b/test/test_endpoints.py
index b29db6af5..e520b3b37 100644
--- a/test/test_endpoints.py
+++ b/test/test_endpoints.py
@@ -8,6 +8,7 @@ import base64
 from urllib import urlencode
 from urlparse import urlparse, urlunparse, parse_qs
 from datetime import datetime, timedelta
+from httmock import urlmatch, HTTMock
 
 import jwt
 
@@ -22,13 +23,25 @@ from endpoints import keyserver
 from endpoints.api import api, api_bp
 from endpoints.api.user import Signin
 from endpoints.keyserver import jwk_with_kid
+from endpoints.csrf import OAUTH_CSRF_TOKEN_NAME
 from endpoints.web import web as web_bp
+from endpoints.oauthlogin import oauthlogin as oauthlogin_bp
 from initdb import setup_database_for_testing, finished_database_for_testing
 from test.helpers import assert_action_logged
 
+try:
+  app.register_blueprint(oauthlogin_bp, url_prefix='/oauth')
+except ValueError:
+  # This blueprint was already registered
+  pass
 
 try:
   app.register_blueprint(web_bp, url_prefix='')
+except ValueError:
+  # This blueprint was already registered
+  pass
+
+try:
   app.register_blueprint(keyserver.key_server, url_prefix='')
 except ValueError:
   # This blueprint was already registered
@@ -69,6 +82,7 @@ class EndpointTestCase(unittest.TestCase):
   def setCsrfToken(self, token):
     with self.app.session_transaction() as sess:
       sess[CSRF_TOKEN_KEY] = token
+      sess[OAUTH_CSRF_TOKEN_NAME] = 'someoauthtoken'
 
   def getResponse(self, resource_name, expected_code=200, **kwargs):
     rv = self.app.get(url_for(resource_name, **kwargs))
@@ -108,6 +122,140 @@ class EndpointTestCase(unittest.TestCase):
     self.assertEquals(rv.status_code, 200)
 
 
+class OAuthLoginTestCase(EndpointTestCase):
+  def invoke_oauth_tests(self, callback_endpoint, attach_endpoint, service_name, service_ident,
+                         new_username):
+    # Test callback.
+    created = self.invoke_oauth_test(callback_endpoint, service_name, service_ident, new_username)
+
+    # Delete the created user.
+    model.user.delete_user(created, [])
+
+    # Test attach.
+    self.login('devtable', 'password')
+    self.invoke_oauth_test(attach_endpoint, service_name, service_ident, 'devtable')
+
+  def invoke_oauth_test(self, endpoint_name, service_name, service_ident, username):
+    # No CSRF.
+    self.getResponse('oauthlogin.' + endpoint_name, expected_code=403)
+
+    # Invalid CSRF.
+    self.getResponse('oauthlogin.' + endpoint_name, state='somestate', expected_code=403)
+
+    # Valid CSRF, invalid code.
+    self.getResponse('oauthlogin.' + endpoint_name, state='someoauthtoken',
+                     code='invalidcode', expected_code=400)
+
+    # Valid CSRF, valid code.
+    self.getResponse('oauthlogin.' + endpoint_name, state='someoauthtoken',
+                     code='somecode', expected_code=302)
+
+    # Ensure the user was added/modified.
+    found_user = model.user.get_user(username)
+    self.assertIsNotNone(found_user)
+
+    federated_login = model.user.lookup_federated_login(found_user, service_name)
+    self.assertIsNotNone(federated_login)
+    self.assertEquals(federated_login.service_ident, service_ident)
+    return found_user
+
+  def test_google_oauth(self):
+    @urlmatch(netloc=r'accounts.google.com', path='/o/oauth2/token')
+    def account_handler(_, request):
+      if request.body.find("code=somecode") > 0:
+        content = {'access_token': 'someaccesstoken'}
+        return py_json.dumps(content)
+      else:
+        return {'status_code': 400, 'content': '{"message": "Invalid code"}'}
+
+    @urlmatch(netloc=r'www.googleapis.com', path='/oauth2/v1/userinfo')
+    def user_handler(_, __):
+      content = {
+        'id': 'someid',
+        'email': 'someemail@example.com',
+        'verified_email': True,
+      }
+      return py_json.dumps(content)
+
+    with HTTMock(account_handler, user_handler):
+      self.invoke_oauth_tests('google_oauth_callback', 'google_oauth_attach', 'google',
+                              'someid', 'someemail')
+
+  def test_github_oauth(self):
+    @urlmatch(netloc=r'github.com', path='/login/oauth/access_token')
+    def account_handler(url, _):
+      if url.query.find("code=somecode") > 0:
+        content = {'access_token': 'someaccesstoken'}
+        return py_json.dumps(content)
+      else:
+        return {'status_code': 400, 'content': '{"message": "Invalid code"}'}
+
+    @urlmatch(netloc=r'github.com', path='/api/v3/user')
+    def user_handler(_, __):
+      content = {
+        'id': 'someid',
+        'login': 'someusername'
+      }
+      return py_json.dumps(content)
+
+    @urlmatch(netloc=r'github.com', path='/api/v3/user/emails')
+    def email_handler(_, __):
+      content = [{
+        'email': 'someemail@example.com',
+        'verified': True,
+        'primary': True,
+      }]
+      return py_json.dumps(content)
+
+    with HTTMock(account_handler, email_handler, user_handler):
+      self.invoke_oauth_tests('github_oauth_callback', 'github_oauth_attach', 'github',
+                              'someid', 'someusername')
+
+  def test_dex_oauth(self):
+    # TODO(jschorr): Add tests for invalid and expired keys.
+
+    # Generate a public/private key pair for the OIDC transaction.
+    private_key = RSA.generate(2048)
+    jwk = RSAKey(key=private_key.publickey()).serialize()
+    token = jwt.encode({
+      'iss': 'https://oidcserver/',
+      'aud': 'someclientid',
+      'sub': 'someid',
+      'exp': int(time.time()) + 60,
+      'iat': int(time.time()),
+      'nbf': int(time.time()),
+      'email': 'someemail@example.com',
+      'email_verified': True,
+    }, private_key.exportKey('PEM'), 'RS256')
+
+    @urlmatch(netloc=r'oidcserver', path='/.well-known/openid-configuration')
+    def wellknown_handler(url, _):
+      return py_json.dumps({
+        'authorization_endpoint': 'http://oidcserver/auth',
+        'token_endpoint': 'http://oidcserver/token',
+        'jwks_uri': 'http://oidcserver/keys',
+      })
+
+    @urlmatch(netloc=r'oidcserver', path='/token')
+    def account_handler(url, request):
+      if request.body.find("code=somecode") > 0:
+        return py_json.dumps({
+          'access_token': token,
+        })
+      else:
+        return {'status_code': 400, 'content': '{"message": "Invalid code"}'}
+
+    @urlmatch(netloc=r'oidcserver', path='/keys')
+    def keys_handler(_, __):
+      return py_json.dumps({
+        "keys": [jwk],
+      })
+
+    with HTTMock(wellknown_handler, account_handler, keys_handler):
+      self.invoke_oauth_tests('dex_oauth_callback', 'dex_oauth_attach', 'dex',
+                              'someid', 'someemail')
+
+
 class WebEndpointTestCase(EndpointTestCase):
   def test_index(self):
     self.getResponse('web.index')
diff --git a/test/testconfig.py b/test/testconfig.py
index aee1b902f..02c678200 100644
--- a/test/testconfig.py
+++ b/test/testconfig.py
@@ -75,3 +75,12 @@ class TestConfig(DefaultConfig):
   INSTANCE_SERVICE_KEY_LOCATION = 'test/data/test.pem'
 
   PROMETHEUS_AGGREGATOR_URL = None
+
+  FEATURE_GITHUB_LOGIN = True
+  FEATURE_GOOGLE_LOGIN = True
+  FEATURE_DEX_LOGIN = True
+
+  DEX_LOGIN_CONFIG = {
+    'CLIENT_ID': 'someclientid',
+    'OIDC_SERVER': 'https://oidcserver/',
+  }
diff --git a/util/config/oauth.py b/util/config/oauth.py
index 6b1ef9b9b..44bf084f2 100644
--- a/util/config/oauth.py
+++ b/util/config/oauth.py
@@ -4,6 +4,11 @@ import logging
 import time
 
 from cachetools import TTLCache
+from cachetools.func import lru_cache
+
+from cryptography.hazmat.backends import default_backend
+from cryptography.hazmat.primitives.serialization import load_der_public_key
+
 from jwkest.jwk import KEYS
 from util import slash_join
 
@@ -64,12 +69,14 @@ class OAuthConfig(object):
     else:
       get_access_token = http_client.post(token_url, params=payload, headers=headers, auth=auth)
 
+    if get_access_token.status_code / 100 != 2:
+      return None
+
     json_data = get_access_token.json()
     if not json_data:
-      return ''
+      return None
 
-    token = json_data.get('access_token', '')
-    return token
+    return json_data.get('access_token', None)
 
 
 class GithubOAuthConfig(OAuthConfig):
@@ -265,11 +272,15 @@ class OIDCConfig(OAuthConfig):
     super(OIDCConfig, self).__init__(config, key_name)
 
     self._public_key_cache = TTLCache(1, PUBLIC_KEY_CACHE_TTL, missing=self._get_public_key)
-    self._oidc_config = {}
+    self._config = config
     self._http_client = config['HTTPCLIENT']
 
+  @lru_cache(maxsize=1)
+  def _oidc_config(self):
     if self.config.get('OIDC_SERVER'):
-      self._load_via_discovery(config.get('DEBUGGING', False))
+      return self._load_via_discovery(self._config.get('DEBUGGING', False))
+    else:
+      return {}
 
   def _load_via_discovery(self, is_debugging):
     oidc_server = self.config['OIDC_SERVER']
@@ -283,16 +294,16 @@ class OIDCConfig(OAuthConfig):
       raise Exception("Could not load OIDC discovery information")
 
     try:
-      self._oidc_config = json.loads(discovery.text)
+      return json.loads(discovery.text)
     except ValueError:
       logger.exception('Could not parse OIDC discovery for url: %s', discovery_url)
       raise Exception("Could not parse OIDC discovery information")
 
   def authorize_endpoint(self):
-    return self._oidc_config.get('authorization_endpoint', '') + '?'
+    return self._oidc_config().get('authorization_endpoint', '') + '?'
 
   def token_endpoint(self):
-    return self._oidc_config.get('token_endpoint')
+    return self._oidc_config().get('token_endpoint')
 
   def user_endpoint(self):
     return None
@@ -322,9 +333,9 @@ class OIDCConfig(OAuthConfig):
     # a random key chose to be stored in the cache, and could be anything.
     return self._public_key_cache[None]
 
-  def _get_public_key(self):
+  def _get_public_key(self, _):
     """ Retrieves the public key for this handler. """
-    keys_url = self._oidc_config['jwks_uri']
+    keys_url = self._oidc_config()['jwks_uri']
 
     keys = KEYS()
     keys.load_from_url(keys_url)
@@ -334,7 +345,10 @@ class OIDCConfig(OAuthConfig):
 
     rsa_key = list(keys)[0]
     rsa_key.deserialize()
-    return rsa_key.key.exportKey('PEM')
+
+    # Reload the key so that we can give a key *instance* to PyJWT to work around its weird parsing
+    # issues.
+    return load_der_public_key(rsa_key.key.exportKey('DER'), backend=default_backend())
 
 
 class DexOAuthConfig(OIDCConfig):