diff --git a/spec/Middlewares.spec.js b/spec/Middlewares.spec.js
index 7091206729..7079898160 100644
--- a/spec/Middlewares.spec.js
+++ b/spec/Middlewares.spec.js
@@ -412,4 +412,27 @@ describe('middlewares', () => {
     middlewares.handleParseHeaders(fakeReq, fakeRes);
     expect(fakeRes.status).toHaveBeenCalledWith(403);
   });
+
+  it('should success without x-parse-application-id in header when there is only one app', (done) => {
+    AppCache.del('test');
+    delete fakeReq.body._ApplicationId;
+    middlewares.handleParseHeaders(fakeReq, fakeRes, () => {
+      expect(fakeRes.status).not.toHaveBeenCalled();
+      done();
+    });
+  });
+  it('should success with x-parse-application-id match an app when there are multiple apps', (done) => {
+    fakeReq.headers['x-parse-application-id'] = fakeReq.body._ApplicationId;
+    delete fakeReq.body._ApplicationId;
+    middlewares.handleParseHeaders(fakeReq, fakeRes, () => {
+      expect(fakeRes.status).not.toHaveBeenCalled();
+      done();
+    });
+  });
+  it('should faile with x-parse-application-id not match any app when there are multiple apps', () => {
+    fakeReq.headers['x-parse-application-id'] = 'do-not-match-an-app';
+    delete fakeReq.body._ApplicationId;
+    middlewares.handleParseHeaders(fakeReq, fakeRes);
+    expect(fakeRes.status).toHaveBeenCalledWith(403);
+  });
 });
diff --git a/src/middlewares.js b/src/middlewares.js
index 526372ba39..ba7c4e52eb 100644
--- a/src/middlewares.js
+++ b/src/middlewares.js
@@ -49,73 +49,59 @@ export function handleParseHeaders(req, res, next) {
     }
   }
 
+  var fileViaJSON = false;
+
+  // To support client SDKs that always POST instead of use proper HTTP calls,
+  // try parse req.body Buffer as JSON and read _ApplicationId and other keys from it
+  if (!info.appId && req.body instanceof Buffer) {
+    try {
+      req.body = JSON.parse(req.body);
+      fileViaJSON = true;
+    } catch (e) {
+      // Happens when upload non JSON file to /parse/file endpoint
+    }
+  }
+
+  // Remove certain things sent by client
   if (req.body) {
     // Unity SDK sends a _noBody key which needs to be removed.
     // Unclear at this point if action needs to be taken.
     delete req.body._noBody;
+    // _Revocable Session should always be ignored
+    // https://github.com/parse-community/parse-server/issues/1548
+    delete req.body._RevocableSession;
   }
 
-  var fileViaJSON = false;
-
-  if (!info.appId || !AppCache.get(info.appId)) {
-    // See if we can find the app id on the body.
-    if (req.body instanceof Buffer) {
-      // The only chance to find the app id is if this is a file
-      // upload that actually is a JSON body. So try to parse it.
-      // https://github.com/parse-community/parse-server/issues/6589
-      // It is also possible that the client is trying to upload a file but forgot
-      // to provide x-parse-app-id in header and parse a binary file will fail
-      try {
-        req.body = JSON.parse(req.body);
-      } catch (e) {
-        return invalidRequest(req, res);
-      }
-      fileViaJSON = true;
+  if (req.body && req.body._ApplicationId) {
+    info.appId = req.body._ApplicationId;
+    delete req.body._ApplicationId;
+    info.javascriptKey = req.body._JavaScriptKey || '';
+    delete req.body._JavaScriptKey;
+    // TODO: test that the REST API formats generated by the other
+    // SDKs are handled ok
+    if (req.body._ClientVersion) {
+      info.clientVersion = req.body._ClientVersion;
+      delete req.body._ClientVersion;
     }
-
-    if (req.body) {
-      delete req.body._RevocableSession;
+    if (req.body._InstallationId) {
+      info.installationId = req.body._InstallationId;
+      delete req.body._InstallationId;
     }
-
-    if (
-      req.body &&
-      req.body._ApplicationId &&
-      AppCache.get(req.body._ApplicationId) &&
-      (!info.masterKey ||
-        AppCache.get(req.body._ApplicationId).masterKey === info.masterKey)
-    ) {
-      info.appId = req.body._ApplicationId;
-      info.javascriptKey = req.body._JavaScriptKey || '';
-      delete req.body._ApplicationId;
-      delete req.body._JavaScriptKey;
-      // TODO: test that the REST API formats generated by the other
-      // SDKs are handled ok
-      if (req.body._ClientVersion) {
-        info.clientVersion = req.body._ClientVersion;
-        delete req.body._ClientVersion;
-      }
-      if (req.body._InstallationId) {
-        info.installationId = req.body._InstallationId;
-        delete req.body._InstallationId;
-      }
-      if (req.body._SessionToken) {
-        info.sessionToken = req.body._SessionToken;
-        delete req.body._SessionToken;
-      }
-      if (req.body._MasterKey) {
-        info.masterKey = req.body._MasterKey;
-        delete req.body._MasterKey;
-      }
-      if (req.body._context && req.body._context instanceof Object) {
-        info.context = req.body._context;
-        delete req.body._context;
-      }
-      if (req.body._ContentType) {
-        req.headers['content-type'] = req.body._ContentType;
-        delete req.body._ContentType;
-      }
-    } else {
-      return invalidRequest(req, res);
+    if (req.body._SessionToken) {
+      info.sessionToken = req.body._SessionToken;
+      delete req.body._SessionToken;
+    }
+    if (req.body._MasterKey) {
+      info.masterKey = req.body._MasterKey;
+      delete req.body._MasterKey;
+    }
+    if (req.body._context && req.body._context instanceof Object) {
+      info.context = req.body._context;
+      delete req.body._context;
+    }
+    if (req.body._ContentType) {
+      req.headers['content-type'] = req.body._ContentType;
+      delete req.body._ContentType;
     }
   }
 
@@ -136,8 +122,24 @@ export function handleParseHeaders(req, res, next) {
 
   const clientIp = getClientIp(req);
 
-  info.app = AppCache.get(info.appId);
-  req.config = Config.get(info.appId, mount);
+  let appId;
+  if (info.appId) {
+    // Request provided appId, just use that
+    appId = info.appId;
+  } else if (Object.keys(AppCache.cache).length === 1) {
+    // Request did not provide appId, but there is only one app anyway, just use that
+    appId = Object.keys(AppCache.cache)[0];
+  } else {
+    // Request did not provide appId and there are multiple apps, we do not know which one to use
+    return invalidRequest(req, res);
+  }
+
+  info.app = AppCache.get(appId);
+  if (!info.app) {
+    // The appId user provided is not valid
+    return invalidRequest(req, res);
+  }
+  req.config = Config.get(appId, mount);
   req.config.headers = req.headers || {};
   req.config.ip = clientIp;
   req.info = info;