diff --git a/core/server/services/url/utils.js b/core/server/services/url/utils.js
index f7319ac5fd..dec5617fb8 100644
--- a/core/server/services/url/utils.js
+++ b/core/server/services/url/utils.js
@@ -6,7 +6,7 @@ const moment = require('moment-timezone'),
     cheerio = require('cheerio'),
     config = require('../../config'),
     settingsCache = require('../settings/cache'),
-    BASE_API_PATH = '/ghost/api/',
+    BASE_API_PATH = '/ghost/api',
     STATIC_IMAGE_URL_PREFIX = 'content/images';
 
 /**
@@ -16,6 +16,17 @@ const moment = require('moment-timezone'),
  * @return {string} API Path for version
  */
 function getApiPath(options) {
+    const versionPath = getVersionPath(options);
+    return `${BASE_API_PATH}${versionPath}`;
+}
+
+/**
+ * Returns path containing only the path for the specific version asked or deprecated by default
+ * @param {Object} options {version} for which to get the path(stable, actice, deprecated),
+ * {type} admin|content: defaults to {version: deprecated, type: content}
+ * @return {string} API version path
+ */
+function getVersionPath(options) {
     const apiVersions = config.get('api:versions');
     let requestedVersion = options.version || 'deprecated';
     let requestedVersionType = options.type || 'content';
@@ -24,7 +35,7 @@ function getApiPath(options) {
         versionData = apiVersions[versionData];
     }
     let versionPath = versionData[requestedVersionType];
-    return `${BASE_API_PATH}${versionPath}/`;
+    return `/${versionPath}/`;
 }
 
 /**
@@ -466,6 +477,7 @@ module.exports.redirect301 = redirect301;
 module.exports.createUrl = createUrl;
 module.exports.deduplicateDoubleSlashes = deduplicateDoubleSlashes;
 module.exports.getApiPath = getApiPath;
+module.exports.getVersionPath = getVersionPath;
 module.exports.getBlogUrl = getBlogUrl;
 
 /**
diff --git a/core/server/web/api/index.js b/core/server/web/api/index.js
new file mode 100644
index 0000000000..a89eef55d9
--- /dev/null
+++ b/core/server/web/api/index.js
@@ -0,0 +1,21 @@
+const debug = require('ghost-ignition').debug('web:api:default:app');
+const express = require('express');
+const urlUtils = require('../../services/url/utils');
+const errorHandler = require('../shared/middlewares/error-handler');
+
+module.exports = function setupApiApp() {
+    debug('Parent API setup start');
+    const apiApp = express();
+
+    // Mount different API versions
+    apiApp.use(urlUtils.getVersionPath({version: 'v0.1'}), require('./v0.1/app')());
+    apiApp.use(urlUtils.getVersionPath({version: 'v2', type: 'content'}), require('./v2/content/app')());
+    apiApp.use(urlUtils.getVersionPath({version: 'v2', type: 'admin'}), require('./v2/admin/app')());
+
+    // Error handling for requests to non-existent API versions
+    apiApp.use(errorHandler.resourceNotFound);
+    apiApp.use(errorHandler.handleJSONResponse);
+
+    debug('Parent API setup end');
+    return apiApp;
+};
\ No newline at end of file
diff --git a/core/server/web/parent-app.js b/core/server/web/parent-app.js
index d9245b8479..75bccd681f 100644
--- a/core/server/web/parent-app.js
+++ b/core/server/web/parent-app.js
@@ -4,7 +4,6 @@ const config = require('../config');
 const compress = require('compression');
 const netjet = require('netjet');
 const shared = require('./shared');
-const urlUtils = require('../services/url/utils');
 
 module.exports = function setupParentApp(options = {}) {
     debug('ParentApp setup start');
@@ -36,11 +35,10 @@ module.exports = function setupParentApp(options = {}) {
     parentApp.use(shared.middlewares.ghostLocals);
 
     // Mount the  apps on the parentApp
+
     // API
     // @TODO: finish refactoring the API app
-    parentApp.use(urlUtils.getApiPath({version: 'v0.1'}), require('./api/v0.1/app')());
-    parentApp.use(urlUtils.getApiPath({version: 'v2', type: 'content'}), require('./api/v2/content/app')());
-    parentApp.use(urlUtils.getApiPath({version: 'v2', type: 'admin'}), require('./api/v2/admin/app')());
+    parentApp.use('/ghost/api', require('./api')());
 
     // ADMIN
     parentApp.use('/ghost', require('./admin')());
diff --git a/core/test/unit/web/parent-app_spec.js b/core/test/unit/web/parent-app_spec.js
index 658b77923a..79c914ba37 100644
--- a/core/test/unit/web/parent-app_spec.js
+++ b/core/test/unit/web/parent-app_spec.js
@@ -6,9 +6,7 @@ var should = require('should'),
 describe('parent app', function () {
     let expressStub;
     let use;
-    let apiV01Spy;
-    let apiContentV2Spy;
-    let apiAdminV2Spy;
+    let apiSpy;
     let parentApp;
     let adminSpy;
     let siteSpy;
@@ -20,17 +18,13 @@ describe('parent app', function () {
             enable: () => {}
         });
 
-        apiV01Spy = sinon.spy();
-        apiContentV2Spy = sinon.spy();
-        apiAdminV2Spy = sinon.spy();
+        apiSpy = sinon.spy();
         adminSpy = sinon.spy();
         siteSpy = sinon.spy();
 
         parentApp = proxyquire('../../../server/web/parent-app', {
             express: expressStub,
-            './api/v0.1/app': apiV01Spy,
-            './api/v2/content/app': apiContentV2Spy,
-            './api/v2/admin/app': apiAdminV2Spy,
+            './api': apiSpy,
             './admin': adminSpy,
             './site': siteSpy
         });
@@ -40,17 +34,13 @@ describe('parent app', function () {
         sandbox.restore();
     });
 
-    it('should mount 5 apps and assign correct routes to them', function () {
+    it('should mount 3 apps and assign correct routes to them', function () {
         parentApp();
 
-        use.calledWith('/ghost/api/v0.1/').should.be.true();
-        use.calledWith('/ghost/api/v2/content/').should.be.true();
-        use.calledWith('/ghost/api/v2/admin/').should.be.true();
+        use.calledWith('/ghost/api').should.be.true();
         use.calledWith('/ghost').should.be.true();
 
-        apiV01Spy.called.should.be.true();
-        apiContentV2Spy.called.should.be.true();
-        apiAdminV2Spy.called.should.be.true();
+        apiSpy.called.should.be.true();
         adminSpy.called.should.be.true();
         siteSpy.called.should.be.true();
     });