diff --git a/server/routes.ts b/server/routes.ts
index 08bfb9b77fb..fea905fc0a7 100644
--- a/server/routes.ts
+++ b/server/routes.ts
@@ -307,7 +307,31 @@ export default async (app: express.Application) => {
     },
   };
 
-  app.use('/graphql', graphqlUploadExpress());
+  // Wrap graphqlUploadExpress with error handling to provide better error messages
+  // for multipart upload parsing failures (see https://github.com/opencollective/opencollective-api/issues/11293)
+  app.use('/graphql', (req, res, next) => {
+    const uploadMiddleware = graphqlUploadExpress();
+    uploadMiddleware(req, res, (err?: Error) => {
+      if (err) {
+        logger.error(`GraphQL upload error: ${err.message}`, { error: err });
+        // Return a proper JSON error response instead of letting Express error handler return a generic 500
+        return res.status(400).json({
+          errors: [
+            {
+              message: `File upload failed: ${err.message}`,
+              extensions: {
+                code: 'BAD_REQUEST',
+                exception: {
+                  name: err.name,
+                },
+              },
+            },
+          ],
+        });
+      }
+      next();
+    });
+  });
 
   /**
    * GraphQL v1
diff --git a/test/server/routes/graphql.test.ts b/test/server/routes/graphql.test.ts
index b717d2e0c28..5acee84d899 100644
--- a/test/server/routes/graphql.test.ts
+++ b/test/server/routes/graphql.test.ts
@@ -219,3 +219,85 @@ describe('GraphQL Armor Protection Tests', () => {
     });
   });
 });
+
+describe('GraphQL Multipart Upload Error Handling', () => {
+  let app;
+
+  before(async () => {
+    app = await startTestServer();
+  });
+
+  after(async () => {
+    await stopTestServer();
+  });
+
+  describe('/graphql/v2', () => {
+    it('should return errors in GraphQL format for malformed multipart requests', async () => {
+      // Send a multipart request with invalid JSON in the operations field.
+      // This triggers an error in graphqlUploadExpress middleware.
+      // See: https://github.com/opencollective/opencollective-api/issues/11293
+      const boundary = '----WebKitFormBoundary7MA4YWxkTrZu0gW';
+      const body = [
+        `--${boundary}`,
+        'Content-Disposition: form-data; name="operations"',
+        '',
+        '{ invalid json }', // Invalid JSON triggers parsing error in graphqlUploadExpress
+        `--${boundary}`,
+        'Content-Disposition: form-data; name="map"',
+        '',
+        '{}',
+        `--${boundary}--`,
+      ].join('\r\n');
+
+      const response = await request(app)
+        .post('/graphql/v2')
+        .set('Content-Type', `multipart/form-data; boundary=${boundary}`)
+        .set('Authorization', 'Bearer test-token')
+        .send(body);
+
+      // The error should be returned in GraphQL format (errors array) not Express format (error object)
+      // This is important because GraphQL clients expect the standard errors array format.
+      expect(response.status).to.eq(400);
+      expect(response.body.errors).to.exist;
+      expect(response.body.errors).to.be.an('array');
+      expect(response.body.errors[0].message).to.include('File upload failed');
+    });
+
+    it('should return GraphQL response (not 500) for valid multipart upload requests', async () => {
+      // Send a valid multipart upload request following GraphQL multipart spec.
+      // Even if auth fails, the response should be in GraphQL format, not a raw 500.
+      // See: https://github.com/opencollective/opencollective-api/issues/11293
+      const response = await request(app)
+        .post('/graphql/v2')
+        .set('Authorization', 'Bearer test-token')
+        .field(
+          'operations',
+          JSON.stringify({
+            query: `mutation UploadFile($files: [UploadFileInput!]!) {
+              uploadFile(files: $files) { file { id url name } }
+            }`,
+            variables: { files: [{ kind: 'EXPENSE_ITEM', file: null }] },
+          }),
+        )
+        .field('map', JSON.stringify({ '0': ['variables.files.0.file'] }))
+        .attach('0', Buffer.from('test file content'), {
+          filename: 'test.txt',
+          contentType: 'text/plain',
+        });
+
+      // Should NOT return 500 - should return proper GraphQL response
+      // Even if auth fails (401-ish error), it should be in GraphQL format
+      expect(response.status).to.not.eq(500);
+
+      // If there's an error, it should be in GraphQL format
+      if (response.body.errors) {
+        expect(response.body.errors).to.be.an('array');
+        expect(response.body.errors[0]).to.have.property('message');
+      }
+      // If successful, it should have data
+      if (response.body.data) {
+        expect(response.body.data).to.have.property('uploadFile');
+      }
+    });
+  });
+});