diff --git a/.changeset/curly-teachers-sort.md b/.changeset/curly-teachers-sort.md
new file mode 100644
index 00000000000..73c935a98bc
--- /dev/null
+++ b/.changeset/curly-teachers-sort.md
@@ -0,0 +1,5 @@
+---
+"@rocket.chat/meteor": patch
+---
+
+Fixes a bug where changing site url  breaks `meteor_runtime_config` path until we reset the server
diff --git a/apps/meteor/app/cors/server/cors.ts b/apps/meteor/app/cors/server/cors.ts
index a9d50ee4297..12ec52d0ab0 100644
--- a/apps/meteor/app/cors/server/cors.ts
+++ b/apps/meteor/app/cors/server/cors.ts
@@ -1,4 +1,3 @@
-import { createHash } from 'crypto';
 import type http from 'http';
 import type { UrlWithParsedQuery } from 'url';
 import url from 'url';
@@ -9,6 +8,7 @@ import { Meteor } from 'meteor/meteor';
 import type { StaticFiles } from 'meteor/webapp';
 import { WebApp, WebAppInternals } from 'meteor/webapp';
 
+import { getWebAppHash } from '../../../server/configuration/configureBoilerplate';
 import { settings } from '../../settings/server';
 
 // Taken from 'connect' types
@@ -128,18 +128,9 @@ WebAppInternals.staticFilesMiddleware = function (
 	// a cache of the file for the wrong hash and start a client loop due to the mismatch
 	// of the hashes of ui versions which would be checked against a websocket response
 	if (path === '/meteor_runtime_config.js') {
-		const program = WebApp.clientPrograms[arch] as (typeof WebApp.clientPrograms)[string] & {
-			meteorRuntimeConfigHash?: string;
-			meteorRuntimeConfig: string;
-		};
-
-		if (!program?.meteorRuntimeConfigHash) {
-			program.meteorRuntimeConfigHash = createHash('sha1')
-				.update(JSON.stringify(encodeURIComponent(program.meteorRuntimeConfig)))
-				.digest('hex');
-		}
+		const hash = getWebAppHash(arch);
 
-		if (program.meteorRuntimeConfigHash !== url.query.hash) {
+		if (!hash || hash !== url.query.hash) {
 			res.writeHead(404);
 			return res.end();
 		}
diff --git a/apps/meteor/server/configuration/configureBoilerplate.ts b/apps/meteor/server/configuration/configureBoilerplate.ts
index dbc5bd5e2ba..ca5c949c699 100644
--- a/apps/meteor/server/configuration/configureBoilerplate.ts
+++ b/apps/meteor/server/configuration/configureBoilerplate.ts
@@ -1,13 +1,39 @@
+import { createHash } from 'crypto';
+
 import { Meteor } from 'meteor/meteor';
-import { WebAppInternals } from 'meteor/webapp';
+import { WebApp, WebAppInternals } from 'meteor/webapp';
 
 import type { ICachedSettings } from '../../app/settings/server/CachedSettings';
 
+const webAppHashes: Record<string, string> = {};
+
+export function getWebAppHash(arch: string): string | undefined {
+	if (!webAppHashes[arch]) {
+		const program = WebApp.clientPrograms[arch] as (typeof WebApp.clientPrograms)[string] & {
+			meteorRuntimeConfig: string;
+		};
+		webAppHashes[arch] = createHash('sha1')
+			.update(JSON.stringify(encodeURIComponent(program.meteorRuntimeConfig)))
+			.digest('hex');
+	}
+
+	return webAppHashes[arch];
+}
+
+const { generateBoilerplate } = WebAppInternals;
+
+WebAppInternals.generateBoilerplate = function (...args: Parameters<typeof generateBoilerplate>) {
+	for (const arch of Object.keys(WebApp.clientPrograms)) {
+		delete webAppHashes[arch];
+	}
+	return generateBoilerplate.apply(this, args);
+};
+
 export function configureBoilerplate(settings: ICachedSettings): void {
 	settings.watch<string>(
 		'Site_Url',
 		// Needed as WebAppInternals.generateBoilerplate needs to be called in a fiber
-		Meteor.bindEnvironment((value) => {
+		Meteor.bindEnvironment(async (value) => {
 			if (value == null || value.trim() === '') {
 				return;
 			}
@@ -28,7 +54,7 @@ export function configureBoilerplate(settings: ICachedSettings): void {
 			process.env.MOBILE_ROOT_URL = host;
 			process.env.MOBILE_DDP_URL = host;
 			if (typeof WebAppInternals !== 'undefined' && WebAppInternals.generateBoilerplate) {
-				return WebAppInternals.generateBoilerplate();
+				await WebAppInternals.generateBoilerplate();
 			}
 		}),
 	);
diff --git a/apps/meteor/tests/end-to-end/api/cors.ts b/apps/meteor/tests/end-to-end/api/cors.ts
new file mode 100644
index 00000000000..089c7c78066
--- /dev/null
+++ b/apps/meteor/tests/end-to-end/api/cors.ts
@@ -0,0 +1,72 @@
+import { expect } from 'chai';
+import { after, before, describe, it } from 'mocha';
+
+import { getCredentials, request } from '../../data/api-data';
+import { updateSetting } from '../../data/permissions.helper';
+
+const getHash = () =>
+	request
+		.get('/')
+		.expect(200)
+		.expect('Content-Type', 'text/html; charset=utf-8')
+		.then((res) => {
+			const hashMatch = res.text.match(/meteor_runtime_config\.js\?hash=([^"']+)/);
+			expect(hashMatch).to.not.be.null;
+			const hash = hashMatch![1];
+			return hash;
+		});
+
+describe('[CORS]', () => {
+	before((done) => getCredentials(done));
+	after(async () => {
+		await updateSetting('Site_Url', 'http://localhost:3000');
+	});
+
+	describe('[/meteor_runtime_config.js]', () => {
+		it('should return 404 when hash is missing', (done) => {
+			void request.get('/meteor_runtime_config.js').expect(404).end(done);
+		});
+
+		it('should return 404 when hash is invalid', (done) => {
+			void request.get('/meteor_runtime_config.js').query({ hash: 'invalid_hash' }).expect(404).end(done);
+		});
+
+		it('should return runtime config when hash matches', async () => {
+			// First get the root page to extract the hash
+			const hash = await getHash();
+
+			// Now request with the extracted hash
+			await request
+				.get('/meteor_runtime_config.js')
+				.query({ hash })
+				.expect(200)
+				.expect('Content-Type', 'application/javascript; charset=UTF-8')
+				.expect((res) => {
+					expect(res.text).to.include('__meteor_runtime_config__');
+					expect(res.text).to.include('http://localhost:3000');
+				});
+		});
+
+		it('should return 404 when hash does not match', (done) => {
+			// First get the root page to extract the hash
+			void request.get('/meteor_runtime_config.js').query({ hash: 'invalidHash' }).expect(404).end(done);
+		});
+
+		it('should update hash when ROOT_URL changes', async () => {
+			const originalHash = getHash();
+			await updateSetting('Site_Url', 'http://new-url:3000');
+			const newHash = await getHash();
+			expect(newHash).to.not.equal(originalHash);
+			// it should return if the new hash is valid
+			await request
+				.get('/meteor_runtime_config.js')
+				.query({ hash: newHash })
+				.expect(200)
+				.expect('Content-Type', 'application/javascript; charset=UTF-8')
+				.expect((res) => {
+					expect(res.text).to.include('__meteor_runtime_config__');
+					expect(res.text).to.include('http://new-url:3000');
+				});
+		});
+	});
+});