diff --git a/src/commands/agent-exec.agent-owner.test.ts b/src/commands/agent-exec.agent-owner.test.ts
new file mode 100644
index 000000000000..e7304df812b2
--- /dev/null
+++ b/src/commands/agent-exec.agent-owner.test.ts
@@ -0,0 +1,80 @@
+import fs from "node:fs/promises";
+import path from "node:path";
+import { afterEach, describe, expect, it, vi } from "vitest";
+import { useAutoCleanupTempDirTracker } from "../../test/helpers/temp-dir.js";
+import { resolveSessionStorePathCore } from "../config/sessions/paths.js";
+import { resolveSqliteScope } from "../config/sessions/session-accessor.sqlite-scope.js";
+import type { RuntimeEnv } from "../runtime.js";
+import { agentExecCommand } from "./agent-exec.js";
+
+const tempDirs = useAutoCleanupTempDirTracker(afterEach);
+
+const runtime: RuntimeEnv = {
+  log: vi.fn(),
+  error: vi.fn(),
+  exit: vi.fn(),
+};
+
+afterEach(() => {
+  vi.restoreAllMocks();
+});
+
+describe("agent exec owner selection", () => {
+  it.each([
+    {
+      name: "a migrated legacy default",
+      config: {
+        agents: {
+          entries: {
+            alpha: { default: true },
+            beta: {},
+          },
+        },
+      },
+    },
+    {
+      name: "the canonical system-agent owner",
+      config: {
+        agents: {
+          ownership: "explicit",
+          defaults: { systemAgent: { agentId: "alpha" } },
+          entries: { alpha: {}, beta: {} },
+        },
+      },
+    },
+  ])("uses $name for the run and its SQLite store scope", async ({ config }) => {
+    const configRoot = tempDirs.make("openclaw-agent-exec-default-agent-");
+    const configPath = path.join(configRoot, "openclaw.json");
+    await fs.writeFile(configPath, JSON.stringify(config), "utf8");
+    const runAgent = vi.fn(async (options: Record<string, unknown>) => {
+      const requestedAgentId = typeof options.agentId === "string" ? options.agentId : "main";
+      const sessionId = String(options.sessionId);
+      const storePath = resolveSessionStorePathCore(undefined, {
+        agentId: "alpha",
+        env: process.env,
+      });
+
+      // Exercise the production guard that rejects keys owned by another agent.
+      expect(() =>
+        resolveSqliteScope({
+          agentId: requestedAgentId,
+          defaultAgentId: "alpha",
+          env: process.env,
+          sessionKey: `agent:${requestedAgentId}:explicit:${sessionId}`,
+          storePath,
+        }),
+      ).not.toThrow();
+      expect(requestedAgentId).toBe("alpha");
+      return {
+        payloads: [{ text: "done" }],
+        meta: { durationMs: 1 },
+      };
+    });
+
+    const result = await agentExecCommand("inspect", { config: configPath }, runtime, { runAgent });
+
+    expect(result.envelope.error).toBeUndefined();
+    expect(result.exitCode).toBe(0);
+    expect(runAgent).toHaveBeenCalledOnce();
+  });
+});
diff --git a/src/commands/agent-exec.ts b/src/commands/agent-exec.ts
index 5ea0253dfbac..f8f637484e77 100644
--- a/src/commands/agent-exec.ts
+++ b/src/commands/agent-exec.ts
@@ -635,7 +635,11 @@ export async function agentExecCommand(
     const pluginInstallRoots = pluginInstallContext?.resolvePluginInstallRoots();
     const timeout = normalizeTimeoutSeconds(opts.timeout);
     const fallbacks = normalizeFallbacks(opts.model, opts.fallback);
-    const { resolveDefaultAgentDir } = await import("../agents/agent-scope-config.js");
+    const {
+      resolveAgentDir,
+      resolveSystemAgentTargetAgentId,
+      tryResolveLegacyCompatibilityAgentId,
+    } = await import("../agents/agent-scope-config.js");
     // Resolve from the inherited config, not `{}`: the default agent may declare
     // its own `agentDir`, and that is where its stored auth profiles live. This
     // reads `baseConfig` rather than `runConfig` because the run config
@@ -643,7 +647,15 @@ export async function agentExecCommand(
     // credential ownership must still follow the operator's configuration.
     // Computed before the environment repoints the state dir so the unconfigured
     // case still resolves against the real one.
-    const storedAuthAgentDir = resolveDefaultAgentDir(baseConfig);
+    const execAgentId =
+      tryResolveLegacyCompatibilityAgentId(baseConfig) ??
+      resolveSystemAgentTargetAgentId(baseConfig, undefined, {
+        surface: "agent exec",
+        hint: "Set agents.defaults.systemAgent.agentId.",
+      });
+    // Auth, session keys, and SQLite ownership must share one resolved owner.
+    // Splitting these paths can select an agent's store but emit a `main` key.
+    const storedAuthAgentDir = resolveAgentDir(baseConfig, execAgentId);
     restoreEnvironment = setAgentExecEnvironment({ stateDir, cwd });
     runtimePaths = await import("../config/paths.js");
     runtimePaths.pinRuntimePaths();
@@ -698,6 +710,7 @@ export async function agentExecCommand(
         {
           message: prompt,
           sessionId,
+          agentId: execAgentId,
           workspaceDir: cwd,
           cwd,
           model: opts.model,