diff --git a/.changeset/angry-poems-build.md b/.changeset/angry-poems-build.md
new file mode 100644
index 00000000000..46b9abc38d8
--- /dev/null
+++ b/.changeset/angry-poems-build.md
@@ -0,0 +1,5 @@
+---
+'@rocket.chat/meteor': patch
+---
+
+Fixes incorrect message sender for incoming webhooks when "Post As" field is updated by ensuring both username and userId are synced to reflect the selected user.
diff --git a/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts b/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts
index 2f45a6c9f72..774d7a0d597 100644
--- a/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts
+++ b/apps/meteor/app/integrations/server/methods/incoming/updateIncomingIntegration.ts
@@ -23,18 +23,14 @@ declare module '@rocket.chat/ddp-client' {
 	}
 }
 
-export const updateIncomingIntegration = async (
-	userId: string,
-	integrationId: string,
-	integration: INewIncomingIntegration | IUpdateIncomingIntegration,
-): Promise<IIntegration | null> => {
-	if (!integration.channel || typeof integration.channel.valueOf() !== 'string' || integration.channel.trim() === '') {
+function validateChannels(channelString: string | undefined): string[] {
+	if (!channelString || typeof channelString.valueOf() !== 'string' || channelString.trim() === '') {
 		throw new Meteor.Error('error-invalid-channel', 'Invalid channel', {
 			method: 'updateIncomingIntegration',
 		});
 	}
 
-	const channels = integration.channel.split(',').map((channel) => channel.trim());
+	const channels = channelString.split(',').map((channel) => channel.trim());
 
 	for (const channel of channels) {
 		if (!validChannelChars.includes(channel[0])) {
@@ -44,6 +40,16 @@ export const updateIncomingIntegration = async (
 		}
 	}
 
+	return channels;
+}
+
+export const updateIncomingIntegration = async (
+	userId: string,
+	integrationId: string,
+	integration: INewIncomingIntegration | IUpdateIncomingIntegration,
+): Promise<IIntegration | null> => {
+	const channels = validateChannels(integration.channel);
+
 	let currentIntegration;
 
 	if (await hasPermissionAsync(userId, 'manage-incoming-integrations')) {
@@ -153,7 +159,8 @@ export const updateIncomingIntegration = async (
 		}
 	}
 
-	const user = await Users.findOne({ username: currentIntegration.username });
+	const username = 'username' in integration ? integration.username : currentIntegration.username;
+	const user = await Users.findOne({ username });
 
 	if (!user?._id) {
 		throw new Meteor.Error('error-invalid-post-as-user', 'Invalid Post As User', {
@@ -173,7 +180,7 @@ export const updateIncomingIntegration = async (
 				emoji: integration.emoji,
 				alias: integration.alias,
 				channel: channels,
-				...('username' in integration && { username: integration.username }),
+				...('username' in integration && { username: user.username, userId: user._id }),
 				...(isFrozen
 					? {}
 					: {
@@ -188,6 +195,7 @@ export const updateIncomingIntegration = async (
 				_updatedBy: await Users.findOne({ _id: userId }, { projection: { username: 1 } }),
 			},
 		},
+		{ returnDocument: 'after' },
 	);
 
 	if (updatedIntegration) {
diff --git a/apps/meteor/app/integrations/server/methods/outgoing/updateOutgoingIntegration.ts b/apps/meteor/app/integrations/server/methods/outgoing/updateOutgoingIntegration.ts
index 2df3dfcb13f..29b150a6001 100644
--- a/apps/meteor/app/integrations/server/methods/outgoing/updateOutgoingIntegration.ts
+++ b/apps/meteor/app/integrations/server/methods/outgoing/updateOutgoingIntegration.ts
@@ -106,6 +106,7 @@ export const updateOutgoingIntegration = async (
 						},
 					}),
 		},
+		{ returnDocument: 'after' },
 	);
 
 	if (updatedIntegration) {
diff --git a/apps/meteor/tests/end-to-end/api/incoming-integrations.ts b/apps/meteor/tests/end-to-end/api/incoming-integrations.ts
index f745bf34cc3..3e8769adda0 100644
--- a/apps/meteor/tests/end-to-end/api/incoming-integrations.ts
+++ b/apps/meteor/tests/end-to-end/api/incoming-integrations.ts
@@ -1,5 +1,6 @@
 import type { Credentials } from '@rocket.chat/api-client';
 import type { IIntegration, IMessage, IRoom, IUser } from '@rocket.chat/core-typings';
+import { Random } from '@rocket.chat/random';
 import { assert, expect } from 'chai';
 import { after, before, describe, it } from 'mocha';
 
@@ -606,6 +607,16 @@ describe('[Incoming Integrations]', () => {
 	});
 
 	describe('[/integrations.update]', () => {
+		let senderUser: IUser;
+		let sendUserCredentials: Credentials;
+
+		before(async () => {
+			senderUser = await createUser();
+			sendUserCredentials = await login(senderUser.username, password);
+		});
+
+		after(() => deleteUser(senderUser));
+
 		it('should update an integration by id and return the new data', (done) => {
 			void request
 				.put(api('integrations.update'))
@@ -629,6 +640,7 @@ describe('[Incoming Integrations]', () => {
 					expect(res.body.integration._id).to.be.equal(integration._id);
 					expect(res.body.integration.name).to.be.equal('Incoming test updated');
 					expect(res.body.integration.alias).to.be.equal('test updated');
+					integration = res.body.integration;
 				})
 				.end(done);
 		});
@@ -649,6 +661,60 @@ describe('[Incoming Integrations]', () => {
 				})
 				.end(done);
 		});
+
+		it("should update an integration's username and associated userId correctly and return the new data", async () => {
+			await request
+				.put(api('integrations.update'))
+				.set(credentials)
+				.send({
+					type: 'webhook-incoming',
+					name: 'Incoming test updated x2',
+					enabled: true,
+					alias: 'test updated x2',
+					username: senderUser.username,
+					scriptEnabled: true,
+					overrideDestinationChannelEnabled: true,
+					channel: '#general',
+					integrationId: integration._id,
+				})
+				.expect('Content-Type', 'application/json')
+				.expect(200)
+				.expect((res) => {
+					expect(res.body).to.have.property('success', true);
+					expect(res.body).to.have.property('integration');
+					expect(res.body.integration._id).to.be.equal(integration._id);
+					expect(res.body.integration.name).to.be.equal('Incoming test updated x2');
+					expect(res.body.integration.alias).to.be.equal('test updated x2');
+					expect(res.body.integration.username).to.be.equal(senderUser.username);
+					expect(res.body.integration.userId).to.be.equal(sendUserCredentials['X-User-Id']);
+					integration = res.body.integration;
+				});
+		});
+
+		it('should send messages to the channel under the updated username', async () => {
+			const successfulMesssage = `Message sent successfully at #${Random.id()}`;
+			await request
+				.post(`/hooks/${integration._id}/${integration.token}`)
+				.send({
+					text: successfulMesssage,
+				})
+				.expect(200);
+
+			await request
+				.get(api('channels.messages'))
+				.set(credentials)
+				.query({
+					roomId: 'GENERAL',
+				})
+				.expect('Content-Type', 'application/json')
+				.expect(200)
+				.expect((res) => {
+					expect(res.body).to.have.property('success', true);
+					expect(res.body).to.have.property('messages').and.to.be.an('array');
+					const message = (res.body.messages as IMessage[]).find((m) => m.msg === successfulMesssage);
+					expect(message?.u).have.property('username', senderUser.username);
+				});
+		});
 	});
 
 	describe('[/integrations.remove]', () => {