diff --git a/api/src/app.ts b/api/src/app.ts
index 21f7c04790a..fa2dbf68154 100644
--- a/api/src/app.ts
+++ b/api/src/app.ts
@@ -105,7 +105,10 @@ export const build = async (
     // test environments)
     skipInit: !SENTRY_DSN,
     errorResponse: (error, _request, reply) => {
-      if (reply.statusCode === 500) {
+      const isCSRFError =
+        error.code === 'FST_CSRF_INVALID_TOKEN' ||
+        error.code === 'FST_CSRF_MISSING_SECRET';
+      if (reply.statusCode === 500 || isCSRFError) {
         void reply.send({
           message: 'flash.generic-error',
           type: 'danger'
diff --git a/api/src/routes/challenge.ts b/api/src/routes/challenge.ts
index 096450d6c43..b29fcfc7b2a 100644
--- a/api/src/routes/challenge.ts
+++ b/api/src/routes/challenge.ts
@@ -396,8 +396,7 @@ export const challengeRoutes: FastifyPluginCallbackTypebox = (
         !multifileCertProjectIds.includes(challengeId) &&
         !multifilePythonCertProjectIds.includes(challengeId)
       ) {
-        void reply.code(403);
-        return 'That challenge type is not saveable.';
+        void reply.code(403).send('That challenge type is not saveable.');
       }
 
       const userSavedChallenges = saveUserChallengeData(
@@ -413,7 +412,7 @@ export const challengeRoutes: FastifyPluginCallbackTypebox = (
         }
       });
 
-      return { savedChallenges: userSavedChallenges };
+      void reply.send({ savedChallenges: userSavedChallenges });
     }
   );
 
diff --git a/api/src/routes/settings.test.ts b/api/src/routes/settings.test.ts
index a82a3c4847e..23aa8abc70c 100644
--- a/api/src/routes/settings.test.ts
+++ b/api/src/routes/settings.test.ts
@@ -62,10 +62,8 @@ describe('settingRoutes', () => {
       });
 
       expect(response.body).toEqual({
-        code: 'FST_CSRF_MISSING_SECRET',
-        error: 'Forbidden',
-        message: 'Missing csrf secret',
-        statusCode: 403
+        message: 'flash.generic-error',
+        type: 'danger'
       });
       expect(response.statusCode).toEqual(403);
     });
@@ -76,10 +74,8 @@ describe('settingRoutes', () => {
       }).set('Cookie', ['_csrf=foo', 'csrf-token=bar']);
 
       expect(response.body).toEqual({
-        code: 'FST_CSRF_INVALID_TOKEN',
-        error: 'Forbidden',
-        message: 'Invalid csrf token',
-        statusCode: 403
+        message: 'flash.generic-error',
+        type: 'danger'
       });
       expect(response.statusCode).toEqual(403);
     });
diff --git a/api/src/schemas/certificate/cert-slug.ts b/api/src/schemas/certificate/cert-slug.ts
index 425834994ac..402fb2fac40 100644
--- a/api/src/schemas/certificate/cert-slug.ts
+++ b/api/src/schemas/certificate/cert-slug.ts
@@ -1,6 +1,6 @@
 import { Type } from '@fastify/type-provider-typebox';
 import { Certification } from '../../../../shared/config/certification-settings';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const certSlug = {
   params: Type.Object({
@@ -120,6 +120,6 @@ export const certSlug = {
         })
       )
     }),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/schemas/certificate/certificate-verify.ts b/api/src/schemas/certificate/certificate-verify.ts
index a790154ea6d..9825544a89b 100644
--- a/api/src/schemas/certificate/certificate-verify.ts
+++ b/api/src/schemas/certificate/certificate-verify.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500, isCertMap } from '../types';
+import { genericError, isCertMap } from '../types';
 
 export const certificateVerify = {
   // TODO(POST_MVP): Remove partial validation from route for schema validation
@@ -126,7 +126,8 @@ export const certificateVerify = {
         type: Type.Literal('danger'),
         message: Type.Literal('flash.went-wrong')
       }),
-      generic500
-    ])
+      genericError
+    ]),
+    default: genericError
   }
 };
diff --git a/api/src/schemas/challenge/backend-challenge-completed.ts b/api/src/schemas/challenge/backend-challenge-completed.ts
index e42149be78b..65a2a2617db 100644
--- a/api/src/schemas/challenge/backend-challenge-completed.ts
+++ b/api/src/schemas/challenge/backend-challenge-completed.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const backendChallengeCompleted = {
   body: Type.Object({
@@ -17,6 +17,6 @@ export const backendChallengeCompleted = {
         'That does not appear to be a valid challenge submission.'
       )
     }),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/schemas/challenge/coderoad-challenge-completed.ts b/api/src/schemas/challenge/coderoad-challenge-completed.ts
index 8bdf5ee0c91..f8ba0e2ed1e 100644
--- a/api/src/schemas/challenge/coderoad-challenge-completed.ts
+++ b/api/src/schemas/challenge/coderoad-challenge-completed.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const coderoadChallengeCompleted = {
   body: Type.Object({
@@ -15,6 +15,6 @@ export const coderoadChallengeCompleted = {
       type: Type.Literal('error'),
       msg: Type.String()
     }),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/schemas/challenge/exam-challenge-completed.ts b/api/src/schemas/challenge/exam-challenge-completed.ts
index 5fa51db497f..af161ee8447 100644
--- a/api/src/schemas/challenge/exam-challenge-completed.ts
+++ b/api/src/schemas/challenge/exam-challenge-completed.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { examResults } from '../types';
+import { examResults, genericError } from '../types';
 
 export const examChallengeCompleted = {
   body: Type.Object({
@@ -30,9 +30,12 @@ export const examChallengeCompleted = {
     400: Type.Object({
       error: Type.String()
     }),
-    403: Type.Object({
-      error: Type.String()
-    }),
+    403: Type.Union([
+      Type.Object({
+        error: Type.String()
+      }),
+      genericError
+    ]),
     500: Type.Object({
       error: Type.String()
     })
diff --git a/api/src/schemas/challenge/exam.ts b/api/src/schemas/challenge/exam.ts
index dec30384e03..ca48befe526 100644
--- a/api/src/schemas/challenge/exam.ts
+++ b/api/src/schemas/challenge/exam.ts
@@ -1,4 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
+import { genericError } from '../types';
 
 export const exam = {
   params: Type.Object({
@@ -27,9 +28,12 @@ export const exam = {
     400: Type.Object({
       error: Type.String()
     }),
-    403: Type.Object({
-      error: Type.String()
-    }),
+    403: Type.Union([
+      Type.Object({
+        error: Type.String()
+      }),
+      genericError
+    ]),
     500: Type.Object({
       error: Type.String()
     })
diff --git a/api/src/schemas/challenge/modern-challenge-completed.ts b/api/src/schemas/challenge/modern-challenge-completed.ts
index 5e71d9575dc..da6c5d8fddb 100644
--- a/api/src/schemas/challenge/modern-challenge-completed.ts
+++ b/api/src/schemas/challenge/modern-challenge-completed.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500, savedChallenge } from '../types';
+import { genericError, savedChallenge } from '../types';
 
 export const modernChallengeCompleted = {
   body: Type.Object({
@@ -30,6 +30,6 @@ export const modernChallengeCompleted = {
         'That does not appear to be a valid challenge submission.'
       )
     }),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/schemas/challenge/project-completed.ts b/api/src/schemas/challenge/project-completed.ts
index 60969db825d..d7230c2baad 100644
--- a/api/src/schemas/challenge/project-completed.ts
+++ b/api/src/schemas/challenge/project-completed.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const projectCompleted = {
   body: Type.Object({
@@ -28,15 +28,20 @@ export const projectCompleted = {
         )
       ])
     }),
-    403: Type.Object({
-      type: Type.Literal('error'),
-      message: Type.Union([
-        Type.Literal(
-          'You have to complete the project before you can submit a URL.'
-        ),
-        Type.Literal('That does not appear to be a valid challenge submission.')
-      ])
-    }),
-    500: generic500
+    403: Type.Union([
+      Type.Object({
+        type: Type.Literal('error'),
+        message: Type.Union([
+          Type.Literal(
+            'You have to complete the project before you can submit a URL.'
+          ),
+          Type.Literal(
+            'That does not appear to be a valid challenge submission.'
+          )
+        ])
+      }),
+      genericError
+    ]),
+    default: genericError
   }
 };
diff --git a/api/src/schemas/challenge/save-challenge.ts b/api/src/schemas/challenge/save-challenge.ts
index 24b987a398e..93b27a8aad8 100644
--- a/api/src/schemas/challenge/save-challenge.ts
+++ b/api/src/schemas/challenge/save-challenge.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { file, generic500, savedChallenge } from '../types';
+import { file, genericError, savedChallenge } from '../types';
 
 export const saveChallenge = {
   body: Type.Object({
@@ -14,7 +14,16 @@ export const saveChallenge = {
     200: Type.Object({
       savedChallenges: Type.Array(savedChallenge)
     }),
-    403: Type.Literal('That challenge type is not saveable.'),
-    500: generic500
+    400: Type.Object({
+      message: Type.Literal(
+        'That does not appear to be a valid challenge submission.'
+      ),
+      type: Type.Literal('error')
+    }),
+    403: Type.Union([
+      Type.Literal('That challenge type is not saveable.'),
+      genericError
+    ]),
+    default: genericError
   }
 };
diff --git a/api/src/schemas/settings/update-my-classroom-mode.ts b/api/src/schemas/settings/update-my-classroom-mode.ts
index 1427e8eb0c2..76d1db7520f 100644
--- a/api/src/schemas/settings/update-my-classroom-mode.ts
+++ b/api/src/schemas/settings/update-my-classroom-mode.ts
@@ -1,4 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
+import { genericError } from '../types';
 
 export const updateMyClassroomMode = {
   body: Type.Object({
@@ -9,9 +10,12 @@ export const updateMyClassroomMode = {
       message: Type.Literal('flash.classroom-mode-updated'),
       type: Type.Literal('success')
     }),
-    403: Type.Object({
-      message: Type.Literal('flash.wrong-updating'),
-      type: Type.Literal('danger')
-    })
+    403: Type.Union([
+      Type.Object({
+        message: Type.Literal('flash.wrong-updating'),
+        type: Type.Literal('danger')
+      }),
+      genericError
+    ])
   }
 };
diff --git a/api/src/schemas/types.ts b/api/src/schemas/types.ts
index 5dc45a7048c..94e90db0ff7 100644
--- a/api/src/schemas/types.ts
+++ b/api/src/schemas/types.ts
@@ -1,6 +1,6 @@
 import { Type } from '@fastify/type-provider-typebox';
 
-export const generic500 = Type.Object({
+export const genericError = Type.Object({
   message: Type.Literal('flash.generic-error'),
   type: Type.Literal('danger')
 });
diff --git a/api/src/schemas/user/delete-my-account.ts b/api/src/schemas/user/delete-my-account.ts
index c83ed5e2471..8004a7c6aaa 100644
--- a/api/src/schemas/user/delete-my-account.ts
+++ b/api/src/schemas/user/delete-my-account.ts
@@ -1,9 +1,9 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const deleteMyAccount = {
   response: {
     200: Type.Object({}),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/schemas/user/delete-user-token.ts b/api/src/schemas/user/delete-user-token.ts
index 3012ed56c00..5ddfa8c2248 100644
--- a/api/src/schemas/user/delete-user-token.ts
+++ b/api/src/schemas/user/delete-user-token.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const deleteUserToken = {
   response: {
@@ -10,6 +10,6 @@ export const deleteUserToken = {
       message: Type.Literal('userToken not found'),
       type: Type.Literal('info')
     }),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/schemas/user/post-ms-username.ts b/api/src/schemas/user/post-ms-username.ts
index d8bf2045810..5791871f5af 100644
--- a/api/src/schemas/user/post-ms-username.ts
+++ b/api/src/schemas/user/post-ms-username.ts
@@ -1,4 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
+import { genericError } from '../types';
 
 export const postMsUsername = {
   body: Type.Object({
@@ -16,10 +17,13 @@ export const postMsUsername = {
       type: Type.Literal('error'),
       message: Type.Literal('flash.ms.transcript.link-err-2')
     }),
-    403: Type.Object({
-      type: Type.Literal('error'),
-      message: Type.Literal('flash.ms.transcript.link-err-4')
-    }),
+    403: Type.Union([
+      Type.Object({
+        type: Type.Literal('error'),
+        message: Type.Literal('flash.ms.transcript.link-err-4')
+      }),
+      genericError
+    ]),
     500: Type.Union([
       Type.Object({
         type: Type.Literal('error'),
diff --git a/api/src/schemas/user/report-user.ts b/api/src/schemas/user/report-user.ts
index 4d19114fa44..f2523b264cf 100644
--- a/api/src/schemas/user/report-user.ts
+++ b/api/src/schemas/user/report-user.ts
@@ -1,5 +1,5 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const reportUser = {
   body: Type.Object({
@@ -18,6 +18,6 @@ export const reportUser = {
       type: Type.Literal('danger'),
       message: Type.Literal('flash.provide-username')
     }),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/schemas/user/reset-my-progress.ts b/api/src/schemas/user/reset-my-progress.ts
index f174c005e77..0dcbb5ca253 100644
--- a/api/src/schemas/user/reset-my-progress.ts
+++ b/api/src/schemas/user/reset-my-progress.ts
@@ -1,9 +1,9 @@
 import { Type } from '@fastify/type-provider-typebox';
-import { generic500 } from '../types';
+import { genericError } from '../types';
 
 export const resetMyProgress = {
   response: {
     200: Type.Object({}),
-    500: generic500
+    default: genericError
   }
 };
diff --git a/api/src/utils/error-formatting.ts b/api/src/utils/error-formatting.ts
index 43a05b3e5f2..3c671d0f926 100644
--- a/api/src/utils/error-formatting.ts
+++ b/api/src/utils/error-formatting.ts
@@ -34,6 +34,8 @@ export const formatProjectCompletedValidation = (
 ): FormattedError => {
   const error = getError(errors);
 
+  // TODO: split this into two functions. There's no need for it to handle both
+  // /project-completed and /save-challenge
   return error.instancePath === '' &&
     error.params.missingProperty === 'solution'
     ? {