diff --git a/core/server/web/shared/middleware/uncapitalise.js b/core/server/web/shared/middleware/uncapitalise.js
index 9c8b644c25..70d0f56ba2 100644
--- a/core/server/web/shared/middleware/uncapitalise.js
+++ b/core/server/web/shared/middleware/uncapitalise.js
@@ -27,13 +27,13 @@ const uncapitalise = (req, res, next) => {
     let decodedURI;
 
     const isSignupOrReset = pathToTest.match(/^(.*\/ghost\/(signup|reset)\/)/i);
-    const isAPI = pathToTest.match(/^(.*\/ghost\/api\/(v[\d.]+|canary)\/.*?\/)/i);
+    const isAPI = pathToTest.match(/^(.*\/ghost\/api(\/(v[\d.]+|canary))?\/.*?\/)/i);
 
     if (isSignupOrReset) {
         pathToTest = isSignupOrReset[1];
     }
 
-    // Do not lowercase anything after e.g. /api/v{X}/ to protect :key/:slug
+    // Do not lowercase anything after e.g. /ghost/api(/v{X})?/ to protect :key/:slug
     if (isAPI) {
         pathToTest = isAPI[1];
     }
diff --git a/test/unit/server/web/shared/middleware/uncapitalise.test.js b/test/unit/server/web/shared/middleware/uncapitalise.test.js
index b82bbb4c2d..d3fdbe9b0e 100644
--- a/test/unit/server/web/shared/middleware/uncapitalise.test.js
+++ b/test/unit/server/web/shared/middleware/uncapitalise.test.js
@@ -127,10 +127,14 @@ describe('Middleware: uncapitalise', function () {
     });
 
     describe('An API request', function () {
-        ['v0.1', 'canary', 'v10'].forEach((apiVersion) => {
+        ['v0.1', 'canary', 'v10', null].forEach((apiVersion) => {
+            const getApiPath = (version) => {
+                return version ? `/${version}` : '';
+            };
+
             describe(`for ${apiVersion}`, function () {
                 it('does nothing if there are no capitals', function (done) {
-                    req.path = `/ghost/api/${apiVersion}/endpoint/`;
+                    req.path = `/ghost/api${getApiPath(apiVersion)}/endpoint/`;
                     uncapitalise(req, res, next);
 
                     next.calledOnce.should.be.true();
@@ -138,32 +142,38 @@ describe('Middleware: uncapitalise', function () {
                 });
 
                 it('version identifier is uppercase', function (done) {
-                    req.path = `/ghost/api/${apiVersion.toUpperCase()}/endpoint/`;
+                    // CASE: capitalizing "empty" string does not make sense
+                    if (apiVersion === null) {
+                        done();
+                        return;
+                    }
+
+                    req.path = `/ghost/api${getApiPath(apiVersion).toUpperCase()}/endpoint/`;
                     req.url = req.path;
 
                     uncapitalise(req, res, next);
 
                     next.called.should.be.false();
                     res.redirect.calledOnce.should.be.true();
-                    res.redirect.calledWith(301, `/ghost/api/${apiVersion}/endpoint/`).should.be.true();
+                    res.redirect.calledWith(301, `/ghost/api${getApiPath(apiVersion)}/endpoint/`).should.be.true();
                     done();
                 });
 
                 it('redirects to the lower case slug if there are capitals', function (done) {
-                    req.path = `/ghost/api/${apiVersion}/ASDfJ/`;
+                    req.path = `/ghost/api${getApiPath(apiVersion)}/ASDfJ/`;
                     req.url = req.path;
 
                     uncapitalise(req, res, next);
 
                     next.called.should.be.false();
                     res.redirect.calledOnce.should.be.true();
-                    res.redirect.calledWith(301, `/ghost/api/${apiVersion}/asdfj/`).should.be.true();
+                    res.redirect.calledWith(301, `/ghost/api${getApiPath(apiVersion)}/asdfj/`).should.be.true();
                     done();
                 });
 
                 it('redirects to the lower case slug if there are capitals in req.baseUrl', function (done) {
                     req.baseUrl = '/Blog';
-                    req.path = `/ghost/api/${apiVersion}/ASDfJ/`;
+                    req.path = `/ghost/api${getApiPath(apiVersion)}/ASDfJ/`;
                     req.url = req.path;
                     req.originalUrl = req.baseUrl + req.path;
 
@@ -171,27 +181,27 @@ describe('Middleware: uncapitalise', function () {
 
                     next.called.should.be.false();
                     res.redirect.calledOnce.should.be.true();
-                    res.redirect.calledWith(301, `/blog/ghost/api/${apiVersion}/asdfj/`).should.be.true();
+                    res.redirect.calledWith(301, `/blog/ghost/api${getApiPath(apiVersion)}/asdfj/`).should.be.true();
                     done();
                 });
 
                 it('does not convert any capitals after the endpoint', function (done) {
                     const query = '?filter=mAgic';
-                    req.path = `/Ghost/API/${apiVersion}/settings/is_private/`;
+                    req.path = `/Ghost/API${getApiPath(apiVersion)}/settings/is_private/`;
                     req.url = `${req.path}${query}`;
 
                     uncapitalise(req, res, next);
 
                     next.called.should.be.false();
                     res.redirect.calledOnce.should.be.true();
-                    res.redirect.calledWith(301, `/ghost/api/${apiVersion}/settings/is_private/${query}`).should.be.true();
+                    res.redirect.calledWith(301, `/ghost/api${getApiPath(apiVersion)}/settings/is_private/${query}`).should.be.true();
                     done();
                 });
 
                 it('does not convert any capitals after the endpoint with baseUrl', function (done) {
                     const query = '?filter=mAgic';
                     req.baseUrl = '/Blog';
-                    req.path = `/ghost/api/${apiVersion}/mail/test@example.COM/`;
+                    req.path = `/ghost/api${getApiPath(apiVersion)}/mail/test@example.COM/`;
                     req.url = `${req.path}${query}`;
                     req.originalUrl = `${req.baseUrl}${req.path}${query}`;
 
@@ -199,7 +209,7 @@ describe('Middleware: uncapitalise', function () {
 
                     next.called.should.be.false();
                     res.redirect.calledOnce.should.be.true();
-                    res.redirect.calledWith(301, `/blog/ghost/api/${apiVersion}/mail/test@example.COM/${query}`).should.be.true();
+                    res.redirect.calledWith(301, `/blog/ghost/api${getApiPath(apiVersion)}/mail/test@example.COM/${query}`).should.be.true();
                     done();
                 });
             });