diff --git a/.changeset/giant-dancers-relate.md b/.changeset/giant-dancers-relate.md
new file mode 100644
index 000000000000..d58385c5da7a
--- /dev/null
+++ b/.changeset/giant-dancers-relate.md
@@ -0,0 +1,5 @@
+---
+"@rocket.chat/meteor": patch
+---
+
+Fixed an `UnhandledPromiseRejection` error on `PUT livechat/departments/:_id` endpoint when `agents` array failed validation
diff --git a/apps/meteor/app/livechat/imports/server/rest/departments.ts b/apps/meteor/app/livechat/imports/server/rest/departments.ts
index 095baefaa294..8355bbd35db7 100644
--- a/apps/meteor/app/livechat/imports/server/rest/departments.ts
+++ b/apps/meteor/app/livechat/imports/server/rest/departments.ts
@@ -110,10 +110,6 @@ API.v1.addRoute(
 			const permissionToSave = await hasPermissionAsync(this.userId, 'manage-livechat-departments');
 			const permissionToAddAgents = await hasPermissionAsync(this.userId, 'add-livechat-department-agents');
 
-			check(this.urlParams, {
-				_id: String,
-			});
-
 			check(this.bodyParams, {
 				department: Object,
 				agents: Match.Maybe(Array),
@@ -128,13 +124,13 @@ API.v1.addRoute(
 			}
 
 			if (success && agents && permissionToAddAgents) {
-				success = Livechat.saveDepartmentAgents(_id, { upsert: agents });
+				success = await Livechat.saveDepartmentAgents(_id, { upsert: agents });
 			}
 
 			if (success) {
 				return API.v1.success({
 					department: await LivechatDepartment.findOneById(_id),
-					agents: await LivechatDepartmentAgents.find({ departmentId: _id }).toArray(),
+					agents: await LivechatDepartmentAgents.findByDepartmentId(_id).toArray(),
 				});
 			}
 
@@ -266,10 +262,6 @@ API.v1.addRoute(
 			return API.v1.success(agents);
 		},
 		async post() {
-			check(this.urlParams, {
-				_id: String,
-			});
-
 			check(
 				this.bodyParams,
 				Match.ObjectIncluding({
diff --git a/apps/meteor/app/livechat/server/lib/Livechat.js b/apps/meteor/app/livechat/server/lib/Livechat.js
index 58a07f00a0d3..35c11ffd3d4f 100644
--- a/apps/meteor/app/livechat/server/lib/Livechat.js
+++ b/apps/meteor/app/livechat/server/lib/Livechat.js
@@ -192,7 +192,6 @@ export const Livechat = {
 	},
 
 	async saveDepartmentAgents(_id, departmentAgents) {
-		check(_id, String);
 		check(departmentAgents, {
 			upsert: Match.Maybe([
 				Match.ObjectIncluding({
@@ -212,7 +211,7 @@ export const Livechat = {
 			]),
 		});
 
-		const department = await LivechatDepartmentRaw.findOneById(_id);
+		const department = await LivechatDepartmentRaw.findOneById(_id, { projection: { enabled: 1 } });
 		if (!department) {
 			throw new Meteor.Error('error-department-not-found', 'Department not found', {
 				method: 'livechat:saveDepartmentAgents',
diff --git a/apps/meteor/tests/end-to-end/api/livechat/10-departments.ts b/apps/meteor/tests/end-to-end/api/livechat/10-departments.ts
index a5a4d848b70d..538ae040fde6 100644
--- a/apps/meteor/tests/end-to-end/api/livechat/10-departments.ts
+++ b/apps/meteor/tests/end-to-end/api/livechat/10-departments.ts
@@ -344,8 +344,15 @@ import { IS_EE } from '../../../e2e/config/constants';
 	});
 
 	describe('PUT livechat/departments/:_id', () => {
+		let department: ILivechatDepartment;
+		before(async () => {
+			department = await createDepartment();
+		});
+		after(async () => {
+			await deleteDepartment(department._id);
+		});
+
 		it('should return an error if fallbackForwardDepartment points to same department', async () => {
-			const department = await createDepartment();
 			await request
 				.put(api(`livechat/department/${department._id}`))
 				.set(credentials)
@@ -361,7 +368,58 @@ import { IS_EE } from '../../../e2e/config/constants';
 				})
 				.expect('Content-Type', 'application/json')
 				.expect(400);
-			await deleteDepartment(department._id);
+		});
+		it('should fail if `agents` param is not an array', async () => {
+			await request
+				.put(api(`livechat/department/${department._id}`))
+				.set(credentials)
+				.send({
+					department: {
+						name: faker.hacker.adjective(),
+						enabled: true,
+						showOnOfflineForm: true,
+						showOnRegistration: true,
+						email: faker.internet.email(),
+					},
+					agents: 'not an array',
+				})
+				.expect('Content-Type', 'application/json')
+				.expect(400);
+		});
+		it('should throw an error if user has permission to add agents and agents array has invalid format', async () => {
+			await updatePermission('add-livechat-department-agents', ['admin']);
+			await request
+				.put(api(`livechat/department/${department._id}`))
+				.set(credentials)
+				.send({
+					department: {
+						name: faker.hacker.adjective(),
+						enabled: true,
+						showOnOfflineForm: true,
+						showOnRegistration: true,
+						email: faker.internet.email(),
+					},
+					agents: [{ notAValidKey: 'string' }],
+				})
+				.expect('Content-Type', 'application/json')
+				.expect(400);
+		});
+		it('should throw an error if user has permission to add agents and agents array has invalid internal format', async () => {
+			await request
+				.put(api(`livechat/department/${department._id}`))
+				.set(credentials)
+				.send({
+					department: {
+						name: faker.hacker.adjective(),
+						enabled: true,
+						showOnOfflineForm: true,
+						showOnRegistration: true,
+						email: faker.internet.email(),
+					},
+					agents: [{ upsert: [{ notAValidKey: 'string' }] }],
+				})
+				.expect('Content-Type', 'application/json')
+				.expect(400);
 		});
 	});