diff --git a/coderd/x/chatd/chattool/createworkspace.go b/coderd/x/chatd/chattool/createworkspace.go
index b57f0e031c..be04be61e4 100644
--- a/coderd/x/chatd/chattool/createworkspace.go
+++ b/coderd/x/chatd/chattool/createworkspace.go
@@ -251,14 +251,6 @@ func CreateWorkspace(organizationID uuid.UUID, db database.Store, options Create
 				}
 			}
 
-			// The agent is now online — re-fire so callers can
-			// load instruction files from the running agent.
-			if options.OnChatUpdated != nil {
-				if latest, err := db.GetChatByID(ctx, options.ChatID); err == nil {
-					options.OnChatUpdated(latest)
-				}
-			}
-
 			result := map[string]any{
 				"created":        true,
 				"workspace_name": workspace.FullName(),
@@ -291,6 +283,19 @@ func CreateWorkspace(organizationID uuid.UUID, db database.Store, options Create
 				}
 			}
 
+			// Re-fire after the agent is fully ready so callers
+			// can load instruction files (AGENTS.md) from the
+			// running agent. This must happen after
+			// waitForAgentReady — firing earlier (e.g. right
+			// after waitForBuild) races with the agent startup
+			// and the connection usually times out before the
+			// agent is reachable.
+			if options.OnChatUpdated != nil {
+				if latest, err := db.GetChatByID(ctx, options.ChatID); err == nil {
+					options.OnChatUpdated(latest)
+				}
+			}
+
 			return toolResponse(result), nil
 		})
 }
diff --git a/coderd/x/chatd/chattool/startworkspace.go b/coderd/x/chatd/chattool/startworkspace.go
index c703cab077..470be41522 100644
--- a/coderd/x/chatd/chattool/startworkspace.go
+++ b/coderd/x/chatd/chattool/startworkspace.go
@@ -134,14 +134,17 @@ func StartWorkspace(options StartWorkspaceOptions) fantasy.AgentTool {
 						build.ID,
 					)), nil
 				}
-				// The agent is now online — re-fire so callers can
-				// load instruction files from the running agent.
+				resp, respErr := waitForAgentAndRespond(ctx, options.DB, options.AgentConnFn, ws, build.ID)
+				// Re-fire after the agent is fully ready so
+				// callers can load instruction files (AGENTS.md).
+				// This must happen after waitForAgentAndRespond —
+				// firing earlier races with agent startup.
 				if options.OnChatUpdated != nil {
 					if latest, err := options.DB.GetChatByID(ctx, options.ChatID); err == nil {
 						options.OnChatUpdated(latest)
 					}
 				}
-				return waitForAgentAndRespond(ctx, options.DB, options.AgentConnFn, ws, build.ID)
+				return resp, respErr
 			case database.ProvisionerJobStatusSucceeded:
 				// If the latest successful build is a start
 				// transition, the workspace should be running.
@@ -197,15 +200,17 @@ func StartWorkspace(options StartWorkspaceOptions) fantasy.AgentTool {
 				)), nil
 			}
 
-			// The agent is now online — re-fire so callers can
-			// load instruction files from the running agent.
+			resp, respErr := waitForAgentAndRespond(ctx, options.DB, options.AgentConnFn, ws, startBuild.ID)
+			// Re-fire after the agent is fully ready so
+			// callers can load instruction files (AGENTS.md).
+			// This must happen after waitForAgentAndRespond —
+			// firing earlier races with agent startup.
 			if options.OnChatUpdated != nil {
 				if latest, err := options.DB.GetChatByID(ctx, options.ChatID); err == nil {
 					options.OnChatUpdated(latest)
 				}
 			}
-
-			return waitForAgentAndRespond(ctx, options.DB, options.AgentConnFn, ws, startBuild.ID)
+			return resp, respErr
 		})
 }