diff --git a/packages/apollo-server-core/CHANGELOG.md b/packages/apollo-server-core/CHANGELOG.md
index a188c3d0e47..03ed98ee7bb 100644
--- a/packages/apollo-server-core/CHANGELOG.md
+++ b/packages/apollo-server-core/CHANGELOG.md
@@ -13,3 +13,4 @@
 * `apollo-server-core`: context creation can be async and errors are formatted to include error code [PR #1024](https://github.com/apollographql/apollo-server/pull/1024)
 * `apollo-server-core`: add `mocks` parameter to the base constructor(applies to all variants) [PR#1017](https://github.com/apollographql/apollo-server/pull/1017)
 * `apollo-server-core`: Remove printing of stack traces with `debug` option and include response in logging function[PR#1018](https://github.com/apollographql/apollo-server/pull/1018)
+* `apollo-server-core`: Returned relevant error codes when an error is thrown by a context function [#1709](https://github.com/apollographql/apollo-server/issues/1709)
diff --git a/packages/apollo-server-core/src/__tests__/runHttpQuery.test.ts b/packages/apollo-server-core/src/__tests__/runHttpQuery.test.ts
index 2f0a1565d0b..840d4bfbc2a 100644
--- a/packages/apollo-server-core/src/__tests__/runHttpQuery.test.ts
+++ b/packages/apollo-server-core/src/__tests__/runHttpQuery.test.ts
@@ -4,6 +4,11 @@ import MockReq = require('mock-req');
 import { GraphQLSchema, GraphQLObjectType, GraphQLString } from 'graphql';
 
 import { runHttpQuery, HttpQueryError } from '../runHttpQuery';
+import {
+  AuthenticationError,
+  ForbiddenError,
+  ValidationError,
+} from 'apollo-server-core';
 
 const queryType = new GraphQLObjectType({
   name: 'QueryType',
@@ -46,4 +51,89 @@ describe('runHttpQuery', () => {
       });
     });
   });
+  describe('error handling in context function', () => {
+    const mockQueryRequest = {
+      method: 'GET',
+      query: {
+        query: '{ testString }',
+      },
+      options: {
+        schema,
+      },
+      request: new MockReq(),
+    };
+
+    it('raises a 401 error if an AuthenticationError is thrown', () => {
+      const noQueryRequest = Object.assign({}, mockQueryRequest, {
+        options: {
+          ...mockQueryRequest.options,
+          context: () => {
+            throw new AuthenticationError('This is the error');
+          },
+        },
+      });
+
+      expect.assertions(2);
+      return runHttpQuery([], noQueryRequest).catch((err: HttpQueryError) => {
+        expect(err.statusCode).toEqual(401);
+        expect(err.message.trim()).toEqual(
+          '{"errors":[{"message":"Context creation failed: This is the error","extensions":{"code":"UNAUTHENTICATED"}}]}',
+        );
+      });
+    });
+    it('raises a 403 error if a ForbiddenError is thrown', () => {
+      const noQueryRequest = Object.assign({}, mockQueryRequest, {
+        options: {
+          ...mockQueryRequest.options,
+          context: () => {
+            throw new ForbiddenError('This is the error');
+          },
+        },
+      });
+
+      expect.assertions(2);
+      return runHttpQuery([], noQueryRequest).catch((err: HttpQueryError) => {
+        expect(err.statusCode).toEqual(403);
+        expect(err.message.trim()).toEqual(
+          '{"errors":[{"message":"Context creation failed: This is the error","extensions":{"code":"FORBIDDEN"}}]}',
+        );
+      });
+    });
+    it('raises a 400 error if any other GraphQL error is thrown', () => {
+      const noQueryRequest = Object.assign({}, mockQueryRequest, {
+        options: {
+          ...mockQueryRequest.options,
+          context: () => {
+            throw new ValidationError('This is the error');
+          },
+        },
+      });
+
+      expect.assertions(2);
+      return runHttpQuery([], noQueryRequest).catch((err: HttpQueryError) => {
+        expect(err.statusCode).toEqual(400);
+        expect(err.message.trim()).toEqual(
+          '{"errors":[{"message":"Context creation failed: This is the error","extensions":{"code":"GRAPHQL_VALIDATION_FAILED"}}]}',
+        );
+      });
+    });
+    it('raises a 500 error if any other error is thrown', () => {
+      const noQueryRequest = Object.assign({}, mockQueryRequest, {
+        options: {
+          ...mockQueryRequest.options,
+          context: () => {
+            throw new Error('This is the error');
+          },
+        },
+      });
+
+      expect.assertions(2);
+      return runHttpQuery([], noQueryRequest).catch((err: HttpQueryError) => {
+        expect(err.statusCode).toEqual(500);
+        expect(err.message.trim()).toEqual(
+          '{"errors":[{"message":"Context creation failed: This is the error","extensions":{"code":"INTERNAL_SERVER_ERROR"}}]}',
+        );
+      });
+    });
+  });
 });
diff --git a/packages/apollo-server-core/src/runHttpQuery.ts b/packages/apollo-server-core/src/runHttpQuery.ts
index 87da2ebd9ee..36826936e0f 100644
--- a/packages/apollo-server-core/src/runHttpQuery.ts
+++ b/packages/apollo-server-core/src/runHttpQuery.ts
@@ -135,6 +135,11 @@ export async function runHttpQuery(
         e.extensions.code &&
         e.extensions.code !== 'INTERNAL_SERVER_ERROR'
       ) {
+        if (e.extensions.code === 'UNAUTHENTICATED') {
+          return throwHttpGraphQLError(401, [e], options);
+        } else if (e.extensions.code === 'FORBIDDEN') {
+          return throwHttpGraphQLError(403, [e], options);
+        }
         return throwHttpGraphQLError(400, [e], options);
       } else {
         return throwHttpGraphQLError(500, [e], options);