diff --git a/core/server/services/api-version-compatibility/index.js b/core/server/services/api-version-compatibility/index.js
index a27f4abdde..46e7872aa3 100644
--- a/core/server/services/api-version-compatibility/index.js
+++ b/core/server/services/api-version-compatibility/index.js
@@ -1,10 +1,13 @@
 const APIVersionCompatibilityService = require('@tryghost/api-version-compatibility-service');
 const VersionNotificationsDataService = require('@tryghost/version-notifications-data-service');
+const versionMismatchHandler = require('@tryghost/mw-api-version-mismatch');
 // const {GhostMailer} = require('../mail');
 const settingsService = require('../../services/settings');
 const models = require('../../models');
 const logging = require('@tryghost/logging');
 
+let serviceInstance;
+
 const init = () => {
     //const ghostMailer = new GhostMailer();
     const versionNotificationsDataService = new VersionNotificationsDataService({
@@ -12,7 +15,7 @@ const init = () => {
         settingsService: settingsService.getSettingsBREADServiceInstance()
     });
 
-    this.APIVersionCompatibilityServiceInstance = new APIVersionCompatibilityService({
+    serviceInstance = new APIVersionCompatibilityService({
         sendEmail: (options) => {
             // NOTE: not using bind here because mockMailer is having trouble mocking bound methods
             //return ghostMailer.send(options);
@@ -25,5 +28,7 @@ const init = () => {
     });
 };
 
-module.exports.APIVersionCompatibilityServiceInstance;
+module.exports.errorHandler = (req, res, next) => {
+    return versionMismatchHandler(serviceInstance)(req, res, next);
+};
 module.exports.init = init;
diff --git a/core/server/web/api/app.js b/core/server/web/api/app.js
index 16cd0d6bf8..aefa175c81 100644
--- a/core/server/web/api/app.js
+++ b/core/server/web/api/app.js
@@ -3,8 +3,7 @@ const config = require('../../../shared/config');
 const express = require('../../../shared/express');
 const sentry = require('../../../shared/sentry');
 const errorHandler = require('@tryghost/mw-error-handler');
-const versionMissmatchHandler = require('@tryghost/mw-api-version-mismatch');
-const {APIVersionCompatibilityServiceInstance} = require('../../services/api-version-compatibility');
+const APIVersionCompatibilityService = require('../../services/api-version-compatibility');
 
 module.exports = function setupApiApp() {
     debug('Parent API setup start');
@@ -32,7 +31,7 @@ module.exports = function setupApiApp() {
 
     // Error handling for requests to non-existent API versions
     apiApp.use(errorHandler.resourceNotFound);
-    apiApp.use(versionMissmatchHandler(APIVersionCompatibilityServiceInstance));
+    apiApp.use(APIVersionCompatibilityService.errorHandler);
     apiApp.use(errorHandler.handleJSONResponseV2(sentry));
 
     debug('Parent API setup end');
diff --git a/core/server/web/api/canary/admin/app.js b/core/server/web/api/canary/admin/app.js
index 6a87c1c026..7a8f77d2d6 100644
--- a/core/server/web/api/canary/admin/app.js
+++ b/core/server/web/api/canary/admin/app.js
@@ -5,10 +5,9 @@ const bodyParser = require('body-parser');
 const shared = require('../../../shared');
 const apiMw = require('../../middleware');
 const errorHandler = require('@tryghost/mw-error-handler');
-const versionMissmatchHandler = require('@tryghost/mw-api-version-mismatch');
 const sentry = require('../../../../../shared/sentry');
 const routes = require('./routes');
-const {APIVersionCompatibilityServiceInstance} = require('../../../../services/api-version-compatibility');
+const APIVersionCompatibilityService = require('../../../../services/api-version-compatibility');
 
 module.exports = function setupApiApp() {
     debug('Admin API canary setup start');
@@ -35,7 +34,7 @@ module.exports = function setupApiApp() {
 
     // API error handling
     apiApp.use(errorHandler.resourceNotFound);
-    apiApp.use(versionMissmatchHandler(APIVersionCompatibilityServiceInstance));
+    apiApp.use(APIVersionCompatibilityService.errorHandler);
     apiApp.use(errorHandler.handleJSONResponseV2(sentry));
 
     debug('Admin API canary setup end');
diff --git a/test/e2e-api/shared/__snapshots__/version.test.js.snap b/test/e2e-api/shared/__snapshots__/version.test.js.snap
index 144e9f3ced..e6fc924fb9 100644
--- a/test/e2e-api/shared/__snapshots__/version.test.js.snap
+++ b/test/e2e-api/shared/__snapshots__/version.test.js.snap
@@ -62,6 +62,62 @@ Object {
 }
 `;
 
+exports[`API Versioning Admin API responds with 406 for an unknown version with accept-version set ahead 1: [body] 1`] = `
+Object {
+  "errors": Array [
+    Object {
+      "code": "UPDATE_GHOST",
+      "context": StringMatching /Provided client version v99\\\\\\.0 is ahead of current Ghost instance version v\\\\d\\+\\\\\\.\\\\d\\+/,
+      "details": null,
+      "help": "Upgrade your Ghost instance.",
+      "id": StringMatching /\\[a-f0-9\\]\\{8\\}-\\[a-f0-9\\]\\{4\\}-\\[a-f0-9\\]\\{4\\}-\\[a-f0-9\\]\\{4\\}-\\[a-f0-9\\]\\{12\\}/,
+      "message": "Request not acceptable for provided Accept-Version header.",
+      "property": null,
+      "type": "RequestNotAcceptableError",
+    },
+  ],
+}
+`;
+
+exports[`API Versioning Admin API responds with 406 for an unknown version with accept-version set ahead 2: [headers] 1`] = `
+Object {
+  "cache-control": "no-cache, private, no-store, must-revalidate, max-stale=0, post-check=0, pre-check=0",
+  "content-length": "347",
+  "content-type": "application/json; charset=utf-8",
+  "etag": StringMatching /\\(\\?:W\\\\/\\)\\?"\\(\\?:\\[ !#-\\\\x7E\\\\x80-\\\\xFF\\]\\*\\|\\\\r\\\\n\\[\\\\t \\]\\|\\\\\\\\\\.\\)\\*"/,
+  "vary": "Accept-Encoding",
+  "x-powered-by": "Express",
+}
+`;
+
+exports[`API Versioning Admin API responds with 406 for an unknown version with accept-version set behind 1: [body] 1`] = `
+Object {
+  "errors": Array [
+    Object {
+      "code": "UPDATE_CLIENT",
+      "context": StringMatching /Provided client version v1\\\\\\.0 is outdated and is behind current Ghost version v\\\\d\\+\\\\\\.\\\\d\\+/,
+      "details": null,
+      "help": "Upgrade your Ghost API client.",
+      "id": StringMatching /\\[a-f0-9\\]\\{8\\}-\\[a-f0-9\\]\\{4\\}-\\[a-f0-9\\]\\{4\\}-\\[a-f0-9\\]\\{4\\}-\\[a-f0-9\\]\\{12\\}/,
+      "message": "Request not acceptable for provided Accept-Version header.",
+      "property": null,
+      "type": "RequestNotAcceptableError",
+    },
+  ],
+}
+`;
+
+exports[`API Versioning Admin API responds with 406 for an unknown version with accept-version set behind 2: [headers] 1`] = `
+Object {
+  "cache-control": "no-cache, private, no-store, must-revalidate, max-stale=0, post-check=0, pre-check=0",
+  "content-length": "354",
+  "content-type": "application/json; charset=utf-8",
+  "etag": StringMatching /\\(\\?:W\\\\/\\)\\?"\\(\\?:\\[ !#-\\\\x7E\\\\x80-\\\\xFF\\]\\*\\|\\\\r\\\\n\\[\\\\t \\]\\|\\\\\\\\\\.\\)\\*"/,
+  "vary": "Accept-Encoding",
+  "x-powered-by": "Express",
+}
+`;
+
 exports[`API Versioning Admin API responds with current content version header when requested version is AHEAD and CAN respond 1: [body] 1`] = `
 Object {
   "site": Object {
diff --git a/test/e2e-api/shared/version.test.js b/test/e2e-api/shared/version.test.js
index 3944c6fbda..cc0669ce5e 100644
--- a/test/e2e-api/shared/version.test.js
+++ b/test/e2e-api/shared/version.test.js
@@ -183,6 +183,34 @@ describe('API Versioning', function () {
                 })
                 .expectEmptyBody();
         });
+
+        it('responds with 406 for an unknown version with accept-version set ahead', async function () {
+            await agentAdminAPI
+                .get('/site/', {baseUrl: '/ghost/api/v99/admin/'})
+                .header('Accept-Version', 'v99.0')
+                .expectStatus(406)
+                .matchHeaderSnapshot({
+                    etag: anyEtag
+                })
+                .matchBodySnapshot({errors: [{
+                    context: stringMatching(/Provided client version v99\.0 is ahead of current Ghost instance version v\d+\.\d+/),
+                    id: anyErrorId
+                }]});
+        });
+
+        it('responds with 406 for an unknown version with accept-version set behind', async function () {
+            await agentAdminAPI
+                .get('/site/', {baseUrl: '/ghost/api/v1/admin/'})
+                .header('Accept-Version', 'v1.0')
+                .expectStatus(406)
+                .matchHeaderSnapshot({
+                    etag: anyEtag
+                })
+                .matchBodySnapshot({errors: [{
+                    context: stringMatching(/Provided client version v1\.0 is outdated and is behind current Ghost version v\d+\.\d+/),
+                    id: anyErrorId
+                }]});
+        });
     });
 
     describe('Content API', function () {