diff --git a/packages/twenty-client-sdk/src/metadata/generated/schema.graphql b/packages/twenty-client-sdk/src/metadata/generated/schema.graphql
index 262f6b5ac9..e5044a483a 100644
--- a/packages/twenty-client-sdk/src/metadata/generated/schema.graphql
+++ b/packages/twenty-client-sdk/src/metadata/generated/schema.graphql
@@ -4703,7 +4703,18 @@ input CreateEmailingDomainInput {
 
 input RunAgentInput {
   agentUniversalIdentifier: String!
-  prompt: String!
+  prompt: String
+  messages: [RunAgentMessageInput!]
+}
+
+input RunAgentMessageInput {
+  role: RunAgentMessageRole!
+  content: String!
+}
+
+enum RunAgentMessageRole {
+  user
+  assistant
 }
 
 input CreateWebhookInput {
diff --git a/packages/twenty-client-sdk/src/metadata/generated/schema.ts b/packages/twenty-client-sdk/src/metadata/generated/schema.ts
index 24e95f96e8..46624ddfdc 100644
--- a/packages/twenty-client-sdk/src/metadata/generated/schema.ts
+++ b/packages/twenty-client-sdk/src/metadata/generated/schema.ts
@@ -3189,6 +3189,8 @@ export interface Mutation {
 
 export type FileFolder = 'CorePicture' | 'AgentChat' | 'BuiltLogicFunction' | 'BuiltFrontComponent' | 'PublicAsset' | 'Source' | 'FilesField' | 'Dependencies' | 'Workflow' | 'EmailAttachment' | 'AppTarball' | 'GeneratedSdkClient' | 'Dpa'
 
+export type RunAgentMessageRole = 'user' | 'assistant'
+
 export type AnalyticsType = 'PAGEVIEW' | 'TRACK'
 
 export interface Subscription {
@@ -6897,7 +6899,9 @@ export interface UpdateEmailGroupChannelInput {id: Scalars['UUID'],displayName?:
 
 export interface CreateEmailingDomainInput {domain: Scalars['String']}
 
-export interface RunAgentInput {agentUniversalIdentifier: Scalars['String'],prompt: Scalars['String']}
+export interface RunAgentInput {agentUniversalIdentifier: Scalars['String'],prompt?: (Scalars['String'] | null),messages?: (RunAgentMessageInput[] | null)}
+
+export interface RunAgentMessageInput {role: RunAgentMessageRole,content: Scalars['String']}
 
 export interface CreateWebhookInput {id?: (Scalars['UUID'] | null),targetUrl: Scalars['String'],operations: Scalars['String'][],description?: (Scalars['String'] | null),secret?: (Scalars['String'] | null)}
 
@@ -9860,6 +9864,11 @@ export const enumFileFolder = {
    Dpa: 'Dpa' as const
 }
 
+export const enumRunAgentMessageRole = {
+   user: 'user' as const,
+   assistant: 'assistant' as const
+}
+
 export const enumAnalyticsType = {
    PAGEVIEW: 'PAGEVIEW' as const,
    TRACK: 'TRACK' as const
diff --git a/packages/twenty-client-sdk/src/metadata/generated/types.ts b/packages/twenty-client-sdk/src/metadata/generated/types.ts
index f0daefdf58..2e6591f4bf 100644
--- a/packages/twenty-client-sdk/src/metadata/generated/types.ts
+++ b/packages/twenty-client-sdk/src/metadata/generated/types.ts
@@ -89,7 +89,8 @@ export default {
         372,
         379,
         380,
-        512
+        492,
+        514
     ],
     "types": {
         "BillingProductDTO": {
@@ -8836,7 +8837,7 @@ export default {
                 308,
                 {
                     "input": [
-                        491,
+                        493,
                         "CreateWebhookInput!"
                     ]
                 }
@@ -8845,7 +8846,7 @@ export default {
                 308,
                 {
                     "input": [
-                        492,
+                        494,
                         "UpdateWebhookInput!"
                     ]
                 }
@@ -8863,7 +8864,7 @@ export default {
                 349,
                 {
                     "input": [
-                        494,
+                        496,
                         "UpdateMessageFolderInput!"
                     ]
                 }
@@ -8872,7 +8873,7 @@ export default {
                 349,
                 {
                     "input": [
-                        496,
+                        498,
                         "UpdateMessageFoldersInput!"
                     ]
                 }
@@ -8881,7 +8882,7 @@ export default {
                 344,
                 {
                     "input": [
-                        497,
+                        499,
                         "UpdateCalendarChannelInput!"
                     ]
                 }
@@ -8890,7 +8891,7 @@ export default {
                 342,
                 {
                     "input": [
-                        499,
+                        501,
                         "SetAppKeyValueInput!"
                     ]
                 }
@@ -8911,7 +8912,7 @@ export default {
                 341,
                 {
                     "input": [
-                        500,
+                        502,
                         "EnqueueJobInput!"
                     ]
                 }
@@ -8941,7 +8942,7 @@ export default {
                         1
                     ],
                     "fileAttachments": [
-                        501,
+                        503,
                         "[FileAttachmentInput!]"
                     ]
                 }
@@ -8970,7 +8971,7 @@ export default {
                         "UUID!"
                     ],
                     "answers": [
-                        502,
+                        504,
                         "[AgentChatQuestionAnswerInput!]!"
                     ],
                     "modelId": [
@@ -9048,7 +9049,7 @@ export default {
                 327,
                 {
                     "input": [
-                        503,
+                        505,
                         "CreateSkillInput!"
                     ]
                 }
@@ -9057,7 +9058,7 @@ export default {
                 327,
                 {
                     "input": [
-                        504,
+                        506,
                         "UpdateSkillInput!"
                     ]
                 }
@@ -9115,7 +9116,7 @@ export default {
                 255,
                 {
                     "input": [
-                        505,
+                        507,
                         "GetAuthorizationUrlForSSOInput!"
                     ]
                 }
@@ -9281,7 +9282,7 @@ export default {
                 258,
                 {
                     "input": [
-                        506
+                        508
                     ]
                 }
             ],
@@ -9456,7 +9457,7 @@ export default {
                 3,
                 {
                     "input": [
-                        507,
+                        509,
                         "UpdateWorkspaceMemberSettingsInput!"
                     ]
                 }
@@ -9490,7 +9491,7 @@ export default {
                 213,
                 {
                     "input": [
-                        508,
+                        510,
                         "SetupOIDCSsoInput!"
                     ]
                 }
@@ -9499,7 +9500,7 @@ export default {
                 213,
                 {
                     "input": [
-                        509,
+                        511,
                         "SetupSAMLSsoInput!"
                     ]
                 }
@@ -9508,7 +9509,7 @@ export default {
                 209,
                 {
                     "input": [
-                        510,
+                        512,
                         "DeleteSsoInput!"
                     ]
                 }
@@ -9517,7 +9518,7 @@ export default {
                 210,
                 {
                     "input": [
-                        511,
+                        513,
                         "EditSsoInput!"
                     ]
                 }
@@ -9546,7 +9547,7 @@ export default {
                 323,
                 {
                     "type": [
-                        512,
+                        514,
                         "AnalyticsType!"
                     ],
                     "name": [
@@ -9589,7 +9590,7 @@ export default {
                 313,
                 {
                     "input": [
-                        513,
+                        515,
                         "CreateCalendarEventInput!"
                     ]
                 }
@@ -9598,7 +9599,7 @@ export default {
                 322,
                 {
                     "input": [
-                        514,
+                        516,
                         "SendEmailInput!"
                     ]
                 }
@@ -9620,7 +9621,7 @@ export default {
                         "String!"
                     ],
                     "connectionParameters": [
-                        516,
+                        518,
                         "EmailAccountConnectionParameters!"
                     ],
                     "id": [
@@ -9632,7 +9633,7 @@ export default {
                 173,
                 {
                     "input": [
-                        518,
+                        520,
                         "UpdateLabPublicFeatureFlagInput!"
                     ]
                 }
@@ -12037,10 +12038,25 @@ export default {
             "prompt": [
                 1
             ],
+            "messages": [
+                491
+            ],
             "__typename": [
                 1
             ]
         },
+        "RunAgentMessageInput": {
+            "role": [
+                492
+            ],
+            "content": [
+                1
+            ],
+            "__typename": [
+                1
+            ]
+        },
+        "RunAgentMessageRole": {},
         "CreateWebhookInput": {
             "id": [
                 4
@@ -12066,7 +12082,7 @@ export default {
                 4
             ],
             "update": [
-                493
+                495
             ],
             "__typename": [
                 1
@@ -12094,7 +12110,7 @@ export default {
                 4
             ],
             "update": [
-                495
+                497
             ],
             "__typename": [
                 1
@@ -12113,7 +12129,7 @@ export default {
                 4
             ],
             "update": [
-                495
+                497
             ],
             "__typename": [
                 1
@@ -12124,7 +12140,7 @@ export default {
                 4
             ],
             "update": [
-                498
+                500
             ],
             "__typename": [
                 1
@@ -12409,7 +12425,7 @@ export default {
                 1
             ],
             "files": [
-                515
+                517
             ],
             "__typename": [
                 1
@@ -12431,13 +12447,13 @@ export default {
                 1
             ],
             "IMAP": [
-                517
+                519
             ],
             "SMTP": [
-                517
+                519
             ],
             "CALDAV": [
-                517
+                519
             ],
             "__typename": [
                 1
@@ -12488,7 +12504,7 @@ export default {
                 243,
                 {
                     "input": [
-                        520,
+                        522,
                         "LogicFunctionLogsInput!"
                     ]
                 }
diff --git a/packages/twenty-docs/developers/extend/apps/logic/skills-and-agents.mdx b/packages/twenty-docs/developers/extend/apps/logic/skills-and-agents.mdx
index b6e7a0b781..15f071fdff 100644
--- a/packages/twenty-docs/developers/extend/apps/logic/skills-and-agents.mdx
+++ b/packages/twenty-docs/developers/extend/apps/logic/skills-and-agents.mdx
@@ -102,7 +102,8 @@ Schema notes:
 
 `runAgent()` lets a logic function run one of your app's agents (with its
 skills and tools). Identify the agent by the `universalIdentifier` you passed
-to `defineAgent()`:
+to `defineAgent()`. Pass either a `prompt` string or a `messages` conversation
+history — not both:
 
 ```ts src/logic-functions/run-enricher.ts
 import { runAgent } from 'twenty-sdk/logic-function';
@@ -113,7 +114,25 @@ const { result, error, success } = await runAgent({
 });
 ```
 
+For multi-turn bots (Slack, Discord, Teams, …), pass thread history as
+`messages` instead of a single `prompt`:
+
+```ts src/logic-functions/reply-in-thread.ts
+import { runAgent } from 'twenty-sdk/logic-function';
+
+const { result, error, success } = await runAgent({
+  agentUniversalIdentifier: 'b3c4d5e6-f7a8-9012-bcde-f34567890123',
+  messages: [
+    { role: 'user', content: 'Who owns Acme?' },
+    { role: 'assistant', content: 'Sarah owns the Acme account.' },
+    { role: 'user', content: 'What was the last touchpoint?' },
+  ],
+});
+```
+
 Key points:
+- Provide **exactly one** of `prompt` (string) or `messages` (1 to 100 entries
+  of `{ role: 'user' | 'assistant', content: string }`).
 - The agent runs **synchronously** and can read/update records itself via its
   own tools — `runAgent()` resolves once the run completes.
 - An app can only run its own agents.
diff --git a/packages/twenty-front/src/generated-metadata/graphql.ts b/packages/twenty-front/src/generated-metadata/graphql.ts
index 0f5b02fce0..07441f2c23 100644
--- a/packages/twenty-front/src/generated-metadata/graphql.ts
+++ b/packages/twenty-front/src/generated-metadata/graphql.ts
@@ -5217,9 +5217,20 @@ export enum RowLevelPermissionPredicateOperand {
 
 export type RunAgentInput = {
   agentUniversalIdentifier: Scalars['String']['input'];
-  prompt: Scalars['String']['input'];
+  messages?: InputMaybe<Array<RunAgentMessageInput>>;
+  prompt?: InputMaybe<Scalars['String']['input']>;
 };
 
+export type RunAgentMessageInput = {
+  content: Scalars['String']['input'];
+  role: RunAgentMessageRole;
+};
+
+export enum RunAgentMessageRole {
+  assistant = 'assistant',
+  user = 'user'
+}
+
 export type RunAgentResult = {
   __typename?: 'RunAgentResult';
   error?: Maybe<Scalars['String']['output']>;
diff --git a/packages/twenty-sdk/src/sdk/logic-function/agents/__tests__/run-agent.spec.ts b/packages/twenty-sdk/src/sdk/logic-function/agents/__tests__/run-agent.spec.ts
index edaaf800a3..d1b2a15f39 100644
--- a/packages/twenty-sdk/src/sdk/logic-function/agents/__tests__/run-agent.spec.ts
+++ b/packages/twenty-sdk/src/sdk/logic-function/agents/__tests__/run-agent.spec.ts
@@ -68,6 +68,42 @@ describe('runAgent', () => {
     });
   });
 
+  it('POSTs messages when provided instead of prompt', async () => {
+    const payload = {
+      result: { response: 'done' },
+      error: null,
+      success: true,
+    };
+
+    fetchSpy.mockResolvedValue(
+      new Response(JSON.stringify({ data: { runAgent: payload } }), {
+        status: 200,
+      }),
+    );
+
+    const messages = [
+      { role: 'user' as const, content: 'Hello' },
+      { role: 'assistant' as const, content: 'Hi' },
+      { role: 'user' as const, content: 'Status?' },
+    ];
+
+    const result = await runAgent({
+      agentUniversalIdentifier: 'agent-uid',
+      messages,
+    });
+
+    expect(result).toEqual(payload);
+
+    const sentBody = JSON.parse(fetchSpy.mock.calls[0][1]?.body as string);
+
+    expect(sentBody.variables).toEqual({
+      input: {
+        agentUniversalIdentifier: 'agent-uid',
+        messages,
+      },
+    });
+  });
+
   it('surfaces GraphQL errors as a regular Error', async () => {
     fetchSpy.mockResolvedValue(
       new Response(
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent-message.input.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent-message.input.ts
new file mode 100644
index 0000000000..9505153f0f
--- /dev/null
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent-message.input.ts
@@ -0,0 +1,18 @@
+import { Field, InputType } from '@nestjs/graphql';
+
+import { IsEnum, IsNotEmpty, IsString } from 'class-validator';
+import { type RunAgentMessage } from 'twenty-shared/application';
+
+import { RunAgentMessageRole } from 'src/engine/metadata-modules/ai/ai-agent-execution/enums/run-agent-message-role.enum';
+
+@InputType('RunAgentMessageInput')
+export class RunAgentMessageInputDTO implements RunAgentMessage {
+  @IsEnum(RunAgentMessageRole)
+  @Field(() => RunAgentMessageRole)
+  role: RunAgentMessageRole;
+
+  @IsString()
+  @IsNotEmpty()
+  @Field()
+  content: string;
+}
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent.input.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent.input.ts
index c021020a18..6094b84f21 100644
--- a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent.input.ts
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent.input.ts
@@ -1,17 +1,37 @@
 import { Field, InputType } from '@nestjs/graphql';
 
-import { IsNotEmpty, IsString } from 'class-validator';
-import { type RunAgentInput } from 'twenty-shared/application';
+import { Type } from 'class-transformer';
+import {
+  ArrayMaxSize,
+  ArrayNotEmpty,
+  IsArray,
+  IsNotEmpty,
+  IsOptional,
+  IsString,
+  ValidateNested,
+} from 'class-validator';
+
+import { RunAgentMessageInputDTO } from 'src/engine/metadata-modules/ai/ai-agent-execution/dtos/run-agent-message.input';
 
 @InputType('RunAgentInput')
-export class RunAgentInputDTO implements RunAgentInput {
+export class RunAgentInputDTO {
   @IsString()
   @IsNotEmpty()
   @Field()
   agentUniversalIdentifier: string;
 
+  @IsOptional()
   @IsString()
   @IsNotEmpty()
-  @Field()
-  prompt: string;
+  @Field({ nullable: true })
+  prompt?: string;
+
+  @IsOptional()
+  @IsArray()
+  @ArrayNotEmpty()
+  @ArrayMaxSize(100)
+  @ValidateNested({ each: true })
+  @Type(() => RunAgentMessageInputDTO)
+  @Field(() => [RunAgentMessageInputDTO], { nullable: true })
+  messages?: RunAgentMessageInputDTO[];
 }
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/enums/run-agent-message-role.enum.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/enums/run-agent-message-role.enum.ts
new file mode 100644
index 0000000000..b573ac2c39
--- /dev/null
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/enums/run-agent-message-role.enum.ts
@@ -0,0 +1,10 @@
+import { registerEnumType } from '@nestjs/graphql';
+
+export enum RunAgentMessageRole {
+  user = 'user',
+  assistant = 'assistant',
+}
+
+registerEnumType(RunAgentMessageRole, {
+  name: 'RunAgentMessageRole',
+});
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-async-executor.service.spec.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-async-executor.service.spec.ts
index ef7afd0727..c0c21f187a 100644
--- a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-async-executor.service.spec.ts
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-async-executor.service.spec.ts
@@ -158,7 +158,7 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
 
     await service.executeAgent({
       agent: buildAgent(),
-      userPrompt: 'test',
+      messages: [{ role: 'user', content: 'test' }],
       baseSystemPrompt: 'base system prompt',
       workspaceId,
     });
@@ -190,7 +190,7 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
 
     await service.executeAgent({
       agent: buildAgent(),
-      userPrompt: 'test',
+      messages: [{ role: 'user', content: 'test' }],
       baseSystemPrompt: 'base system prompt',
       workspaceId,
       toolLoadingStrategy: 'lazy',
@@ -216,7 +216,7 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
 
     await service.executeAgent({
       agent: buildAgent(),
-      userPrompt: 'test',
+      messages: [{ role: 'user', content: 'test' }],
       baseSystemPrompt: 'base system prompt',
       workspaceId,
     });
@@ -224,12 +224,51 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
     expect(toolRegistry.getToolsByCategories).not.toHaveBeenCalled();
   });
 
+  it('passes messages to generateText when messages are provided', async () => {
+    roleTargetRepository.findOne.mockResolvedValueOnce({ roleId: agentRoleId });
+
+    const messages = [
+      { role: 'user' as const, content: 'Hello' },
+      { role: 'assistant' as const, content: 'Hi' },
+      { role: 'user' as const, content: 'Status?' },
+    ];
+
+    await service.executeAgent({
+      agent: buildAgent(),
+      messages,
+      baseSystemPrompt: 'base system prompt',
+      workspaceId,
+    });
+
+    const generateTextArgs = generateTextMock.mock.calls[0][0];
+
+    expect(generateTextArgs.messages).toEqual([
+      { role: 'user', content: 'Hello' },
+      { role: 'assistant', content: 'Hi' },
+      { role: 'user', content: 'Status?' },
+    ]);
+    expect(generateTextArgs).not.toHaveProperty('prompt');
+  });
+
+  it('throws without calling the model when messages are empty', async () => {
+    await expect(
+      service.executeAgent({
+        agent: buildAgent(),
+        messages: [],
+        baseSystemPrompt: 'base system prompt',
+        workspaceId,
+      }),
+    ).rejects.toThrow(/at least one message/);
+
+    expect(generateTextMock).not.toHaveBeenCalled();
+  });
+
   it('prefixes the system prompt with the caller-supplied base prompt', async () => {
     roleTargetRepository.findOne.mockResolvedValueOnce(null);
 
     await service.executeAgent({
       agent: buildAgent(),
-      userPrompt: 'test',
+      messages: [{ role: 'user', content: 'test' }],
       baseSystemPrompt: 'caller base prompt',
       workspaceId,
     });
@@ -264,7 +303,7 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
           schema: { type: 'object', properties: {} },
         },
       } as AgentEntity,
-      userPrompt: 'test',
+      messages: [{ role: 'user', content: 'test' }],
       baseSystemPrompt: AGENT_RUN_BASE_SYSTEM_PROMPT,
       workspaceId,
     });
@@ -302,7 +341,7 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
 
       const result = await service.executeAgent({
         agent: buildAgent(),
-        userPrompt: 'test',
+        messages: [{ role: 'user', content: 'test' }],
         baseSystemPrompt: 'base system prompt',
         workspaceId,
       });
@@ -342,7 +381,7 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
 
       await service.executeAgent({
         agent: buildAgent(),
-        userPrompt: 'test',
+        messages: [{ role: 'user', content: 'test' }],
         baseSystemPrompt: 'base system prompt',
         workspaceId,
       });
@@ -377,7 +416,7 @@ describe('AgentAsyncExecutorService — workflow agent role-scoped tool resoluti
 
       const result = await service.executeAgent({
         agent: buildAgent(),
-        userPrompt: 'test',
+        messages: [{ role: 'user', content: 'test' }],
         baseSystemPrompt: 'base system prompt',
         workspaceId,
       });
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-run.service.spec.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-run.service.spec.ts
index d28d014b48..a3a5d7fc3b 100644
--- a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-run.service.spec.ts
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/__tests__/agent-run.service.spec.ts
@@ -87,6 +87,7 @@ describe('AgentRunService', () => {
 
     expect(agentAsyncExecutorService.executeAgent).toHaveBeenCalledWith(
       expect.objectContaining({
+        messages: [{ role: 'user', content: input.prompt }],
         authContext: {
           type: 'application',
           workspace,
@@ -96,6 +97,81 @@ describe('AgentRunService', () => {
     );
   });
 
+  it('converts a prompt into a single user message', async () => {
+    await service.run({
+      workspace,
+      requestUserWorkspaceId: null,
+      input,
+    });
+
+    expect(
+      agentAsyncExecutorService.executeAgent.mock.calls[0][0].messages,
+    ).toEqual([{ role: 'user', content: input.prompt }]);
+  });
+
+  it('passes messages to the executor when messages are provided instead of prompt', async () => {
+    const messages = [
+      { role: 'user' as const, content: 'Hello' },
+      { role: 'assistant' as const, content: 'Hi there' },
+      { role: 'user' as const, content: 'What is the status?' },
+    ];
+
+    await service.run({
+      workspace,
+      requestUserWorkspaceId: 'user-workspace-1',
+      input: {
+        agentUniversalIdentifier: 'agent-uid',
+        messages,
+      },
+    });
+
+    const executeAgentArgs =
+      agentAsyncExecutorService.executeAgent.mock.calls[0][0];
+
+    expect(executeAgentArgs.messages).toEqual(messages);
+    expect(executeAgentArgs.baseSystemPrompt).toBe(
+      AGENT_RUN_BASE_SYSTEM_PROMPT,
+    );
+    expect(executeAgentArgs.toolLoadingStrategy).toBe('lazy');
+    expect(executeAgentArgs.authContext).toEqual({
+      type: 'application',
+      workspace,
+      application: { id: 'app-1' },
+    });
+  });
+
+  it('throws when neither prompt nor messages are provided', async () => {
+    await expect(
+      service.run({
+        workspace,
+        requestUserWorkspaceId: null,
+        input: {
+          agentUniversalIdentifier: 'agent-uid',
+        },
+      }),
+    ).rejects.toThrow(/exactly one of prompt or messages/);
+
+    expect(agentRepository.findOne).not.toHaveBeenCalled();
+    expect(agentAsyncExecutorService.executeAgent).not.toHaveBeenCalled();
+  });
+
+  it('throws when both prompt and messages are provided', async () => {
+    await expect(
+      service.run({
+        workspace,
+        requestUserWorkspaceId: null,
+        input: {
+          agentUniversalIdentifier: 'agent-uid',
+          prompt: 'Enrich record 123',
+          messages: [{ role: 'user', content: 'Hello' }],
+        },
+      }),
+    ).rejects.toThrow(/exactly one of prompt or messages/);
+
+    expect(agentRepository.findOne).not.toHaveBeenCalled();
+    expect(agentAsyncExecutorService.executeAgent).not.toHaveBeenCalled();
+  });
+
   it('runs the agent with the programmatic base system prompt', async () => {
     await service.run({
       workspace,
@@ -106,6 +182,7 @@ describe('AgentRunService', () => {
     expect(agentAsyncExecutorService.executeAgent).toHaveBeenCalledWith(
       expect.objectContaining({
         baseSystemPrompt: AGENT_RUN_BASE_SYSTEM_PROMPT,
+        toolLoadingStrategy: 'lazy',
       }),
     );
   });
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-async-executor.service.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-async-executor.service.ts
index b33ac6687b..362a4453e2 100644
--- a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-async-executor.service.ts
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-async-executor.service.ts
@@ -5,14 +5,16 @@ import {
   generateText,
   jsonSchema,
   type LanguageModelUsage,
+  type ModelMessage,
   Output,
   stepCountIs,
   type StepResult,
   type ToolSet,
 } from 'ai';
+import { type RunAgentMessage } from 'twenty-shared/application';
 import { AUTO_SELECT_SMART_MODEL_ID } from 'twenty-shared/constants';
 import { type ActorMetadata } from 'twenty-shared/types';
-import { isDefined } from 'twenty-shared/utils';
+import { isDefined, isNonEmptyArray } from 'twenty-shared/utils';
 import { type Repository } from 'typeorm';
 
 import { isUserAuthContext } from 'src/engine/core-modules/auth/guards/is-user-auth-context.guard';
@@ -232,7 +234,7 @@ export class AgentAsyncExecutorService {
 
   async executeAgent({
     agent,
-    userPrompt,
+    messages,
     baseSystemPrompt,
     actorContext,
     authContext,
@@ -242,7 +244,7 @@ export class AgentAsyncExecutorService {
     toolLoadingStrategy = 'preload',
   }: {
     agent: AgentEntity | null;
-    userPrompt: string;
+    messages: RunAgentMessage[];
     baseSystemPrompt: string;
     actorContext?: ActorMetadata;
     authContext?: WorkspaceAuthContext;
@@ -251,6 +253,13 @@ export class AgentAsyncExecutorService {
     operationType?: UsageOperationType;
     toolLoadingStrategy?: AgentToolLoadingStrategy;
   }): Promise<AgentExecutionResult> {
+    if (!isNonEmptyArray(messages)) {
+      throw new AiException(
+        'Provide at least one message to run an agent',
+        AiExceptionCode.INVALID_AGENT_INPUT,
+      );
+    }
+
     await this.billingUsageService.hasAvailableCreditsOrThrow(workspaceId);
 
     let accumulatedUsage: LanguageModelUsage = EMPTY_USAGE;
@@ -348,7 +357,12 @@ export class AgentAsyncExecutorService {
         system: `${baseSystemPrompt}\n\n${agent ? agent.prompt : ''}${toolCatalogSection}`,
         tools,
         model: registeredModel.model,
-        prompt: userPrompt,
+        messages: messages.map(
+          (message): ModelMessage => ({
+            role: message.role,
+            content: message.content,
+          }),
+        ),
         stopWhen: (step) =>
           stepCountIs(AGENT_CONFIG.MAX_STEPS)(step) ||
           hasNoMoreAvailableCredits,
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-run.service.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-run.service.ts
index c6abaf2e91..2f4c2b51b0 100644
--- a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-run.service.ts
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-execution/services/agent-run.service.ts
@@ -1,9 +1,11 @@
 import { Injectable, Logger, NotFoundException } from '@nestjs/common';
 
+import { isNonEmptyString } from '@sniptt/guards';
 import {
-  type RunAgentInput,
+  type RunAgentMessage,
   type RunAgentResult,
 } from 'twenty-shared/application';
+import { isNonEmptyArray } from 'twenty-shared/utils';
 
 import { ApplicationService } from 'src/engine/core-modules/application/application.service';
 import { type WorkspaceAuthContext } from 'src/engine/core-modules/auth/types/workspace-auth-context.type';
@@ -12,9 +14,19 @@ import { type FlatWorkspace } from 'src/engine/core-modules/workspace/types/flat
 import { AgentAsyncExecutorService } from 'src/engine/metadata-modules/ai/ai-agent-execution/services/agent-async-executor.service';
 import { AGENT_RUN_BASE_SYSTEM_PROMPT } from 'src/engine/metadata-modules/ai/ai-agent/constants/agent-run-base-system-prompt.const';
 import { AgentEntity } from 'src/engine/metadata-modules/ai/ai-agent/entities/agent.entity';
+import {
+  AiException,
+  AiExceptionCode,
+} from 'src/engine/metadata-modules/ai/ai.exception';
 import { InjectWorkspaceScopedRepository } from 'src/engine/twenty-orm/workspace-scoped-repository/inject-workspace-scoped-repository.decorator';
 import { WorkspaceScopedRepository } from 'src/engine/twenty-orm/workspace-scoped-repository/workspace-scoped-repository';
 
+type RunAgentServiceInput = {
+  agentUniversalIdentifier: string;
+  prompt?: string | null;
+  messages?: RunAgentMessage[] | null;
+};
+
 @Injectable()
 export class AgentRunService {
   private readonly logger = new Logger(AgentRunService.name);
@@ -33,8 +45,22 @@ export class AgentRunService {
   }: {
     workspace: FlatWorkspace;
     requestUserWorkspaceId: string | null;
-    input: RunAgentInput;
+    input: RunAgentServiceInput;
   }): Promise<RunAgentResult> {
+    const prompt = input.prompt;
+
+    // GraphQL cannot express XOR; enforce exactly one of prompt or messages
+    if (isNonEmptyArray(input.messages) === isNonEmptyString(prompt)) {
+      throw new AiException(
+        'Provide exactly one of prompt or messages',
+        AiExceptionCode.INVALID_AGENT_INPUT,
+      );
+    }
+
+    const messages: RunAgentMessage[] = isNonEmptyString(prompt)
+      ? [{ role: 'user', content: prompt }]
+      : (input.messages ?? []);
+
     const agent = await this.agentRepository.findOne(workspace.id, {
       where: {
         universalIdentifier: input.agentUniversalIdentifier,
@@ -64,19 +90,20 @@ export class AgentRunService {
     };
 
     try {
-      const { result, hasNoMoreAvailableCredits } =
-        await this.agentAsyncExecutorService.executeAgent({
+      const executionResult = await this.agentAsyncExecutorService.executeAgent(
+        {
           agent,
-          userPrompt: input.prompt,
+          messages,
           baseSystemPrompt: AGENT_RUN_BASE_SYSTEM_PROMPT,
           authContext,
           workspaceId: workspace.id,
           userWorkspaceId: requestUserWorkspaceId,
           operationType: UsageOperationType.AI_WORKFLOW_TOKEN,
           toolLoadingStrategy: 'lazy',
-        });
+        },
+      );
 
-      if (hasNoMoreAvailableCredits) {
+      if (executionResult.hasNoMoreAvailableCredits) {
         return {
           result: null,
           error: 'AI agent stopped: no more available credits.',
@@ -84,7 +111,11 @@ export class AgentRunService {
         };
       }
 
-      return { result, error: null, success: true };
+      return {
+        result: executionResult.result,
+        error: null,
+        success: true,
+      };
     } catch (error) {
       this.logger.error(
         `Agent execution failed for ${input.agentUniversalIdentifier}`,
diff --git a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-monitor/jobs/run-evaluation-input.job.ts b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-monitor/jobs/run-evaluation-input.job.ts
index 524ff8bc05..f27dae5dd1 100644
--- a/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-monitor/jobs/run-evaluation-input.job.ts
+++ b/packages/twenty-server/src/engine/metadata-modules/ai/ai-agent-monitor/jobs/run-evaluation-input.job.ts
@@ -56,7 +56,7 @@ export class RunEvaluationInputJob {
 
     const executionResult = await this.aiAgentExecutorService.executeAgent({
       agent,
-      userPrompt: data.input,
+      messages: [{ role: 'user', content: data.input }],
       baseSystemPrompt: AGENT_RUN_BASE_SYSTEM_PROMPT,
       workspaceId: data.workspaceId,
       userWorkspaceId: null,
diff --git a/packages/twenty-server/src/modules/workflow/workflow-executor/workflow-actions/ai-agent/ai-agent.workflow-action.ts b/packages/twenty-server/src/modules/workflow/workflow-executor/workflow-actions/ai-agent/ai-agent.workflow-action.ts
index 055d27d265..3c4871c40c 100644
--- a/packages/twenty-server/src/modules/workflow/workflow-executor/workflow-actions/ai-agent/ai-agent.workflow-action.ts
+++ b/packages/twenty-server/src/modules/workflow/workflow-executor/workflow-actions/ai-agent/ai-agent.workflow-action.ts
@@ -84,7 +84,9 @@ export class AiAgentWorkflowAction implements WorkflowAction {
 
     const executionResult = await this.aiAgentExecutionService.executeAgent({
       agent,
-      userPrompt: resolveInput(prompt, context) as string,
+      messages: [
+        { role: 'user', content: resolveInput(prompt, context) as string },
+      ],
       baseSystemPrompt: WORKFLOW_BASE_SYSTEM_PROMPT,
       actorContext: executionContext.isActingOnBehalfOfUser
         ? executionContext.initiator
diff --git a/packages/twenty-shared/src/application/index.ts b/packages/twenty-shared/src/application/index.ts
index 404fea6c80..07b64f4747 100644
--- a/packages/twenty-shared/src/application/index.ts
+++ b/packages/twenty-shared/src/application/index.ts
@@ -135,7 +135,12 @@ export type {
   RowLevelPermissionPredicateManifest,
   RoleManifest,
 } from './roleManifestType';
-export type { RunAgentInput, RunAgentResult } from './runAgentType';
+export type {
+  RunAgentMessageRole,
+  RunAgentMessage,
+  RunAgentInput,
+  RunAgentResult,
+} from './runAgentType';
 export type { ServerVariables } from './server-variables.type';
 export type { ServerRouteDispatchResult } from './serverRouteDispatchResultType';
 export type { ServerRouteTriggerSettings } from './serverRouteTriggerSettingsType';
diff --git a/packages/twenty-shared/src/application/runAgentType.ts b/packages/twenty-shared/src/application/runAgentType.ts
index e5f1992cd6..3f93cf542e 100644
--- a/packages/twenty-shared/src/application/runAgentType.ts
+++ b/packages/twenty-shared/src/application/runAgentType.ts
@@ -1,7 +1,16 @@
+export type RunAgentMessageRole = 'user' | 'assistant';
+
+export type RunAgentMessage = {
+  role: RunAgentMessageRole;
+  content: string;
+};
+
 export type RunAgentInput = {
   agentUniversalIdentifier: string;
-  prompt: string;
-};
+} & (
+  | { prompt: string; messages?: never }
+  | { messages: RunAgentMessage[]; prompt?: never }
+);
 
 export type RunAgentResult = {
   result: object | null;