diff --git a/backend/internal/daemon/lifecycle_wiring.go b/backend/internal/daemon/lifecycle_wiring.go
index 5113d9dcb6..d8de21df15 100644
--- a/backend/internal/daemon/lifecycle_wiring.go
+++ b/backend/internal/daemon/lifecycle_wiring.go
@@ -109,6 +109,7 @@ func startSession(cfg config.Config, runtime runtimeselect.Runtime, store *sqlit
 		Messenger: messenger,
 		Lifecycle: lcm,
 		DataDir:   cfg.DataDir,
+		RunFile:   cfg.RunFilePath,
 		Logger:    log,
 	})
 	scmProvider, err := newGitHubSCMProvider(log)
diff --git a/backend/internal/session_manager/manager.go b/backend/internal/session_manager/manager.go
index 4a808c24af..ad9448b93f 100644
--- a/backend/internal/session_manager/manager.go
+++ b/backend/internal/session_manager/manager.go
@@ -52,6 +52,13 @@ const (
 	EnvIssueID   = "AO_ISSUE_ID"
 	// EnvDataDir tells a spawned agent's AO hook commands where the store lives.
 	EnvDataDir = "AO_DATA_DIR"
+	// EnvRunFile tells a spawned agent's AO hook commands where the daemon's
+	// running.json handshake lives, so hook delivery finds the SAME daemon that
+	// spawned the session even when AO runs with a non-default state location.
+	// Without it, `ao hooks` falls back to ~/.ao/running.json and every
+	// callback fails against a stale or missing default run file (observed
+	// 2026-07-04: all sessions no_signal, permission dialogs undetected).
+	EnvRunFile = "AO_RUN_FILE"
 )
 
 // hookBinaryName is the executable name the workspace hook commands invoke:
@@ -111,6 +118,7 @@ type Manager struct {
 	messenger ports.AgentMessenger
 	lcm       lifecycleRecorder
 	dataDir   string
+	runFile   string
 	clock     func() time.Time
 	// lookPath is exec.LookPath in production; tests substitute a stub so
 	// they don't need real binaries on PATH. Returns ports.ErrAgentBinaryNotFound
@@ -134,6 +142,9 @@ type Deps struct {
 	// DataDir is exported to spawned agents as AO_DATA_DIR so their hook
 	// commands can open the same store.
 	DataDir string
+	// RunFile is exported to spawned agents as AO_RUN_FILE so their hook
+	// commands locate this daemon's running.json rather than the default.
+	RunFile string
 	Clock   func() time.Time
 	// LookPath overrides exec.LookPath for the pre-launch agent-binary check.
 	// Production wiring leaves this nil and the manager defaults to
@@ -159,6 +170,7 @@ func New(d Deps) *Manager {
 		messenger:  d.Messenger,
 		lcm:        d.Lifecycle,
 		dataDir:    d.DataDir,
+		runFile:    d.RunFile,
 		clock:      d.Clock,
 		lookPath:   d.LookPath,
 		executable: d.Executable,
@@ -1088,8 +1100,8 @@ Keep branch names within your session's branch namespace so AO can track every P
 // spawnEnv builds the runtime environment: the per-project env vars first, then
 // the AO-internal vars last so they always win (a project cannot override
 // AO_SESSION_ID and friends).
-func spawnEnv(id domain.SessionID, project domain.ProjectID, issue domain.IssueID, dataDir string, projectEnv map[string]string) map[string]string {
-	env := make(map[string]string, len(projectEnv)+4)
+func spawnEnv(id domain.SessionID, project domain.ProjectID, issue domain.IssueID, dataDir, runFile string, projectEnv map[string]string) map[string]string {
+	env := make(map[string]string, len(projectEnv)+5)
 	for k, v := range projectEnv {
 		env[k] = v
 	}
@@ -1097,6 +1109,9 @@ func spawnEnv(id domain.SessionID, project domain.ProjectID, issue domain.IssueI
 	env[EnvProjectID] = string(project)
 	env[EnvIssueID] = string(issue)
 	env[EnvDataDir] = dataDir
+	if runFile != "" {
+		env[EnvRunFile] = runFile
+	}
 	return env
 }
 
@@ -1108,7 +1123,7 @@ func spawnEnv(id domain.SessionID, project domain.ProjectID, issue domain.IssueI
 // When the pin cannot be applied the inherited PATH is kept and a warning is
 // logged so the degradation isn't silent.
 func (m *Manager) runtimeEnv(id domain.SessionID, project domain.ProjectID, issue domain.IssueID, projectEnv map[string]string) map[string]string {
-	env := spawnEnv(id, project, issue, m.dataDir, projectEnv)
+	env := spawnEnv(id, project, issue, m.dataDir, m.runFile, projectEnv)
 	path, err := HookPATH(m.executable, os.Getenv, projectEnv)
 	if err != nil {
 		m.logger.Warn("session PATH not pinned to the daemon binary; `ao hooks` callbacks may resolve to a different ao and activity tracking will stall",
diff --git a/backend/internal/session_manager/provision_test.go b/backend/internal/session_manager/provision_test.go
index d82d6e351b..36799e14cc 100644
--- a/backend/internal/session_manager/provision_test.go
+++ b/backend/internal/session_manager/provision_test.go
@@ -11,10 +11,11 @@ import (
 )
 
 func TestSpawnEnvProjectVarsCannotOverrideInternal(t *testing.T) {
-	env := spawnEnv("mer-1", "mer", "issue-9", "/data", map[string]string{
+	env := spawnEnv("mer-1", "mer", "issue-9", "/data", "/state/running.json", map[string]string{
 		"FOO":        "bar",
 		EnvSessionID: "hacked", // a project must not override AO-internal vars
 		EnvProjectID: "hacked",
+		EnvRunFile:   "hacked",
 	})
 	if env["FOO"] != "bar" {
 		t.Fatalf("FOO = %q, want bar", env["FOO"])
@@ -25,6 +26,18 @@ func TestSpawnEnvProjectVarsCannotOverrideInternal(t *testing.T) {
 	if env[EnvProjectID] != "mer" {
 		t.Fatalf("AO_PROJECT_ID = %q, want mer (internal wins)", env[EnvProjectID])
 	}
+	if env[EnvRunFile] != "/state/running.json" {
+		t.Fatalf("AO_RUN_FILE = %q, want /state/running.json (internal wins; hook delivery must find THIS daemon)", env[EnvRunFile])
+	}
+}
+
+// A daemon with no resolved run-file path must not export an empty AO_RUN_FILE
+// (empty would override a useful inherited value with garbage).
+func TestSpawnEnvOmitsEmptyRunFile(t *testing.T) {
+	env := spawnEnv("mer-1", "mer", "", "/data", "", nil)
+	if _, ok := env[EnvRunFile]; ok {
+		t.Fatalf("AO_RUN_FILE exported despite empty run-file path")
+	}
 }
 
 func TestHookPATH(t *testing.T) {