diff --git a/backend/internal/adapters/agent/amp/amp.go b/backend/internal/adapters/agent/amp/amp.go
index efd6430e5..9ceac7b12 100644
--- a/backend/internal/adapters/agent/amp/amp.go
+++ b/backend/internal/adapters/agent/amp/amp.go
@@ -122,6 +122,11 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 	cmd = make([]string, 0, 5)
 	cmd = append(cmd, binary)
 	appendPermissionFlags(&cmd, cfg.Permissions)
+	if cfg.SystemPrompt != "" {
+		cmd = append(cmd, "--append-system-prompt", cfg.SystemPrompt)
+	} else if cfg.SystemPromptFile != "" {
+		cmd = append(cmd, "--append-system-prompt-file", cfg.SystemPromptFile)
+	}
 	cmd = append(cmd, "--resume", agentSessionID)
 	return cmd, true, nil
 }
diff --git a/backend/internal/adapters/agent/amp/amp_test.go b/backend/internal/adapters/agent/amp/amp_test.go
index 68f21b97e..d0045cb95 100644
--- a/backend/internal/adapters/agent/amp/amp_test.go
+++ b/backend/internal/adapters/agent/amp/amp_test.go
@@ -138,7 +138,9 @@ func TestGetRestoreCommand(t *testing.T) {
 		Session: ports.SessionRef{
 			Metadata: map[string]string{ports.MetadataKeyAgentSessionID: "T-abc123"},
 		},
-		Permissions: ports.PermissionModeBypassPermissions,
+		Permissions:      ports.PermissionModeBypassPermissions,
+		SystemPrompt:     "restore inline wins",
+		SystemPromptFile: "/tmp/system.md",
 	})
 	if err != nil {
 		t.Fatal(err)
@@ -147,7 +149,7 @@ func TestGetRestoreCommand(t *testing.T) {
 		t.Fatal("ok=false, want true")
 	}
 
-	want := []string{"amp", "--permission-mode", "bypassPermissions", "--resume", "T-abc123"}
+	want := []string{"amp", "--permission-mode", "bypassPermissions", "--append-system-prompt", "restore inline wins", "--resume", "T-abc123"}
 	if !reflect.DeepEqual(cmd, want) {
 		t.Fatalf("cmd = %#v, want %#v", cmd, want)
 	}
diff --git a/backend/internal/adapters/agent/auggie/auggie.go b/backend/internal/adapters/agent/auggie/auggie.go
index 1ef9f2937..0dc813174 100644
--- a/backend/internal/adapters/agent/auggie/auggie.go
+++ b/backend/internal/adapters/agent/auggie/auggie.go
@@ -152,7 +152,13 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 	if err != nil {
 		return nil, false, err
 	}
-	cmd = []string{binary, "--print", "--resume", agentSessionID}
+	cmd = []string{binary, "--print"}
+	if cfg.SystemPrompt != "" {
+		cmd = append(cmd, "--instruction", cfg.SystemPrompt)
+	} else if cfg.SystemPromptFile != "" {
+		cmd = append(cmd, "--instruction-file", cfg.SystemPromptFile)
+	}
+	cmd = append(cmd, "--resume", agentSessionID)
 	return cmd, true, nil
 }
 
diff --git a/backend/internal/adapters/agent/auggie/auggie_test.go b/backend/internal/adapters/agent/auggie/auggie_test.go
index 8906b1670..1c313bfdb 100644
--- a/backend/internal/adapters/agent/auggie/auggie_test.go
+++ b/backend/internal/adapters/agent/auggie/auggie_test.go
@@ -134,7 +134,9 @@ func TestGetRestoreCommand(t *testing.T) {
 		Session: ports.SessionRef{
 			Metadata: map[string]string{ports.MetadataKeyAgentSessionID: "sess-abc123"},
 		},
-		Permissions: ports.PermissionModeBypassPermissions,
+		Permissions:      ports.PermissionModeBypassPermissions,
+		SystemPrompt:     "restore inline wins",
+		SystemPromptFile: "/tmp/system.md",
 	})
 	if err != nil {
 		t.Fatal(err)
@@ -143,7 +145,7 @@ func TestGetRestoreCommand(t *testing.T) {
 		t.Fatal("ok=false, want true")
 	}
 
-	want := []string{"auggie", "--print", "--resume", "sess-abc123"}
+	want := []string{"auggie", "--print", "--instruction", "restore inline wins", "--resume", "sess-abc123"}
 	if !reflect.DeepEqual(cmd, want) {
 		t.Fatalf("cmd = %#v, want %#v", cmd, want)
 	}
diff --git a/backend/internal/adapters/agent/autohand/autohand.go b/backend/internal/adapters/agent/autohand/autohand.go
index 6fd093192..d7fca5a4d 100644
--- a/backend/internal/adapters/agent/autohand/autohand.go
+++ b/backend/internal/adapters/agent/autohand/autohand.go
@@ -110,8 +110,9 @@ func (p *Plugin) GetPromptDeliveryStrategy(ctx context.Context, cfg ports.Launch
 // GetRestoreCommand rebuilds the argv that continues an existing Autohand
 // session: `autohand resume [--path <workspace>] <sessionId>`. ok is false when
 // the hook-derived native session id has not landed yet, so callers can fall
-// back to fresh launch behavior. Autohand's resume sub-command does not accept
-// approval flags, so none are appended here.
+// back to fresh launch behavior. Autohand's resume sub-command only accepts the
+// workspace path and session id, so approval and system-prompt flags are not
+// re-applied here.
 func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig) (cmd []string, ok bool, err error) {
 	if err := ctx.Err(); err != nil {
 		return nil, false, err
diff --git a/backend/internal/adapters/agent/autohand/autohand_test.go b/backend/internal/adapters/agent/autohand/autohand_test.go
index ddcec5f6d..04b039be0 100644
--- a/backend/internal/adapters/agent/autohand/autohand_test.go
+++ b/backend/internal/adapters/agent/autohand/autohand_test.go
@@ -152,7 +152,8 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	plugin := &Plugin{resolvedBinary: "autohand"}
 
 	cmd, ok, err := plugin.GetRestoreCommand(context.Background(), ports.RestoreConfig{
-		Permissions: ports.PermissionModeAuto,
+		Permissions:  ports.PermissionModeAuto,
+		SystemPrompt: "restore instructions ignored by resume",
 		Session: ports.SessionRef{
 			WorkspacePath: "/work/space",
 			Metadata:      map[string]string{ports.MetadataKeyAgentSessionID: "sess-123"},
diff --git a/backend/internal/adapters/agent/cline/cline.go b/backend/internal/adapters/agent/cline/cline.go
index 512beeb65..21e178309 100644
--- a/backend/internal/adapters/agent/cline/cline.go
+++ b/backend/internal/adapters/agent/cline/cline.go
@@ -122,6 +122,9 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 	cmd = make([]string, 0, 8)
 	cmd = append(cmd, binary, "--json")
 	appendApprovalFlags(&cmd, cfg.Permissions)
+	if cfg.SystemPrompt != "" {
+		cmd = append(cmd, "-s", cfg.SystemPrompt)
+	}
 	cmd = append(cmd, "--id", agentSessionID)
 	return cmd, true, nil
 }
diff --git a/backend/internal/adapters/agent/cline/cline_test.go b/backend/internal/adapters/agent/cline/cline_test.go
index 7b33121f4..e482ac409 100644
--- a/backend/internal/adapters/agent/cline/cline_test.go
+++ b/backend/internal/adapters/agent/cline/cline_test.go
@@ -241,7 +241,8 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	plugin := &Plugin{resolvedBinary: "cline"}
 
 	cmd, ok, err := plugin.GetRestoreCommand(context.Background(), ports.RestoreConfig{
-		Permissions: ports.PermissionModeAuto,
+		Permissions:  ports.PermissionModeAuto,
+		SystemPrompt: "restore instructions",
 		Session: ports.SessionRef{
 			Metadata: map[string]string{ports.MetadataKeyAgentSessionID: "session-123"},
 		},
@@ -256,6 +257,7 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 		"cline",
 		"--json",
 		"--auto-approve", "true",
+		"-s", "restore instructions",
 		"--id", "session-123",
 	}
 	if !reflect.DeepEqual(cmd, want) {
diff --git a/backend/internal/adapters/agent/codex/codex.go b/backend/internal/adapters/agent/codex/codex.go
index 3867efcec..bbb220328 100644
--- a/backend/internal/adapters/agent/codex/codex.go
+++ b/backend/internal/adapters/agent/codex/codex.go
@@ -125,6 +125,11 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 	appendSessionHookFlags(&cmd)
 	appendTerminalCompatibilityFlags(&cmd)
 	appendWorkspaceTrustFlag(&cmd, cfg.Session.WorkspacePath)
+	if cfg.SystemPrompt != "" {
+		cmd = append(cmd, "-c", "developer_instructions="+codexTOMLConfigString(cfg.SystemPrompt))
+	} else if cfg.SystemPromptFile != "" {
+		cmd = append(cmd, "-c", "model_instructions_file="+cfg.SystemPromptFile)
+	}
 	cmd = append(cmd, agentSessionID)
 	return cmd, true, nil
 }
diff --git a/backend/internal/adapters/agent/codex/codex_test.go b/backend/internal/adapters/agent/codex/codex_test.go
index 289feba0e..a8bd58b4a 100644
--- a/backend/internal/adapters/agent/codex/codex_test.go
+++ b/backend/internal/adapters/agent/codex/codex_test.go
@@ -398,7 +398,9 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	workspace := canonicalTempDir(t)
 
 	cmd, ok, err := plugin.GetRestoreCommand(context.Background(), ports.RestoreConfig{
-		Permissions: ports.PermissionModeAuto,
+		Permissions:      ports.PermissionModeAuto,
+		SystemPrompt:     "restore inline wins",
+		SystemPromptFile: filepath.Join("tmp", "restore-system.md"),
 		Session: ports.SessionRef{
 			Metadata:      map[string]string{ports.MetadataKeyAgentSessionID: "thread-123"},
 			WorkspacePath: workspace,
@@ -425,6 +427,7 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	}
 	want = append(want,
 		"-c", `projects={`+codexTOMLConfigString(workspace)+`={trust_level="trusted"}}`,
+		"-c", "developer_instructions="+codexTOMLConfigString("restore inline wins"),
 		"thread-123",
 	)
 	if !reflect.DeepEqual(cmd, want) {
diff --git a/backend/internal/adapters/agent/droid/droid.go b/backend/internal/adapters/agent/droid/droid.go
index 7198d3f27..b306fb94e 100644
--- a/backend/internal/adapters/agent/droid/droid.go
+++ b/backend/internal/adapters/agent/droid/droid.go
@@ -151,6 +151,11 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 		return nil, false, err
 	}
 	cmd = append(cmd, settingsArgs...)
+	if cfg.SystemPrompt != "" {
+		cmd = append(cmd, "--append-system-prompt", cfg.SystemPrompt)
+	} else if cfg.SystemPromptFile != "" {
+		cmd = append(cmd, "--append-system-prompt-file", cfg.SystemPromptFile)
+	}
 	cmd = append(cmd, "-r", agentSessionID)
 	return cmd, true, nil
 }
diff --git a/backend/internal/adapters/agent/droid/droid_test.go b/backend/internal/adapters/agent/droid/droid_test.go
index 2607372c3..ce3ed3607 100644
--- a/backend/internal/adapters/agent/droid/droid_test.go
+++ b/backend/internal/adapters/agent/droid/droid_test.go
@@ -141,6 +141,8 @@ func TestGetLaunchCommandSystemPrompt(t *testing.T) {
 func TestGetRestoreCommand(t *testing.T) {
 	plugin := &Plugin{resolvedBinary: "droid"}
 	cmd, ok, err := plugin.GetRestoreCommand(context.Background(), ports.RestoreConfig{
+		SystemPrompt:     "restore inline wins",
+		SystemPromptFile: "/tmp/system.md",
 		Session: ports.SessionRef{
 			ID: "mer-4",
 			Metadata: map[string]string{
@@ -154,7 +156,7 @@ func TestGetRestoreCommand(t *testing.T) {
 	if !ok {
 		t.Fatal("ok=false, want true")
 	}
-	want := []string{"droid", "-r", "droid-ses-1"}
+	want := []string{"droid", "--append-system-prompt", "restore inline wins", "-r", "droid-ses-1"}
 	if !reflect.DeepEqual(cmd, want) {
 		t.Fatalf("cmd = %#v, want %#v", cmd, want)
 	}
diff --git a/backend/internal/adapters/agent/goose/goose.go b/backend/internal/adapters/agent/goose/goose.go
index 7964a9a86..d1a968139 100644
--- a/backend/internal/adapters/agent/goose/goose.go
+++ b/backend/internal/adapters/agent/goose/goose.go
@@ -142,7 +142,15 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 		return nil, false, err
 	}
 
-	cmd = append(gooseModeEnvPrefix(cfg.Permissions), binary, "run", "--resume", "--session-id", agentSessionID)
+	cmd = append(gooseModeEnvPrefix(cfg.Permissions), binary, "run")
+	systemPrompt, err := restoreSystemPromptText(cfg)
+	if err != nil {
+		return nil, false, err
+	}
+	if systemPrompt != "" {
+		cmd = append(cmd, "--system", systemPrompt)
+	}
+	cmd = append(cmd, "--resume", "--session-id", agentSessionID)
 	return cmd, true, nil
 }
 
@@ -167,17 +175,26 @@ func (p *Plugin) SessionInfo(ctx context.Context, session ports.SessionRef) (por
 // flag takes inline text only (no file variant), so a system-prompt file is read
 // from disk only when inline instructions are unavailable.
 func systemPromptText(cfg ports.LaunchConfig) (string, error) {
-	if cfg.SystemPrompt != "" {
-		return cfg.SystemPrompt, nil
+	return systemPromptTextFrom(cfg.SystemPrompt, cfg.SystemPromptFile)
+}
+
+func restoreSystemPromptText(cfg ports.RestoreConfig) (string, error) {
+	return systemPromptTextFrom(cfg.SystemPrompt, cfg.SystemPromptFile)
+}
+
+func systemPromptTextFrom(inline, file string) (string, error) {
+	if inline != "" {
+		return inline, nil
 	}
-	if cfg.SystemPromptFile != "" {
-		data, err := os.ReadFile(cfg.SystemPromptFile) //nolint:gosec // path is AO-owned launch config
-		if err != nil {
-			return "", fmt.Errorf("read %s: %w", cfg.SystemPromptFile, err)
-		}
-		if text := strings.TrimSpace(string(data)); text != "" {
-			return text, nil
-		}
+	if file == "" {
+		return "", nil
+	}
+	data, err := os.ReadFile(file) //nolint:gosec // path is AO-owned launch config
+	if err != nil {
+		return "", fmt.Errorf("read %s: %w", file, err)
+	}
+	if text := strings.TrimSpace(string(data)); text != "" {
+		return text, nil
 	}
 	return "", nil
 }
diff --git a/backend/internal/adapters/agent/goose/goose_test.go b/backend/internal/adapters/agent/goose/goose_test.go
index 789895424..d40c5fbdb 100644
--- a/backend/internal/adapters/agent/goose/goose_test.go
+++ b/backend/internal/adapters/agent/goose/goose_test.go
@@ -278,7 +278,9 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	plugin := &Plugin{resolvedBinary: "goose"}
 
 	cmd, ok, err := plugin.GetRestoreCommand(context.Background(), ports.RestoreConfig{
-		Permissions: ports.PermissionModeAuto,
+		Permissions:      ports.PermissionModeAuto,
+		SystemPrompt:     "restore inline wins",
+		SystemPromptFile: filepath.Join(t.TempDir(), "missing.md"),
 		Session: ports.SessionRef{
 			Metadata: map[string]string{ports.MetadataKeyAgentSessionID: "thread-123"},
 		},
@@ -291,7 +293,7 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	}
 	want := []string{
 		"env", "GOOSE_MODE=auto",
-		"goose", "run", "--resume", "--session-id", "thread-123",
+		"goose", "run", "--system", "restore inline wins", "--resume", "--session-id", "thread-123",
 	}
 	if !reflect.DeepEqual(cmd, want) {
 		t.Fatalf("restore cmd\nwant: %#v\n got: %#v", want, cmd)
diff --git a/backend/internal/adapters/agent/pi/pi.go b/backend/internal/adapters/agent/pi/pi.go
index e510de671..d00c8c7ae 100644
--- a/backend/internal/adapters/agent/pi/pi.go
+++ b/backend/internal/adapters/agent/pi/pi.go
@@ -146,6 +146,15 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 		return nil, false, err
 	}
 	cmd = []string{binary, "--print", "--session", agentSessionID}
+	if cfg.SystemPrompt != "" {
+		cmd = append(cmd, "--append-system-prompt", cfg.SystemPrompt)
+	} else if cfg.SystemPromptFile != "" {
+		data, err := os.ReadFile(cfg.SystemPromptFile) //nolint:gosec // path is AO-owned launch config
+		if err != nil {
+			return nil, false, err
+		}
+		cmd = append(cmd, "--append-system-prompt", string(data))
+	}
 	return cmd, true, nil
 }
 
diff --git a/backend/internal/adapters/agent/pi/pi_test.go b/backend/internal/adapters/agent/pi/pi_test.go
index 55c728752..0f21e5bc6 100644
--- a/backend/internal/adapters/agent/pi/pi_test.go
+++ b/backend/internal/adapters/agent/pi/pi_test.go
@@ -148,6 +148,8 @@ func TestGetLaunchCommandSystemPromptFileReadError(t *testing.T) {
 func TestGetRestoreCommand(t *testing.T) {
 	p := &Plugin{resolvedBinary: "pi"}
 	cmd, ok, err := p.GetRestoreCommand(context.Background(), ports.RestoreConfig{
+		SystemPrompt:     "restore inline wins",
+		SystemPromptFile: filepath.Join(t.TempDir(), "missing.md"),
 		Session: ports.SessionRef{
 			Metadata: map[string]string{ports.MetadataKeyAgentSessionID: "019e950e-52e0-7411-961b-d380ca7e610f"},
 		},
@@ -160,7 +162,7 @@ func TestGetRestoreCommand(t *testing.T) {
 		t.Fatal("ok=false, want true")
 	}
 
-	want := []string{"pi", "--print", "--session", "019e950e-52e0-7411-961b-d380ca7e610f"}
+	want := []string{"pi", "--print", "--session", "019e950e-52e0-7411-961b-d380ca7e610f", "--append-system-prompt", "restore inline wins"}
 	if !reflect.DeepEqual(cmd, want) {
 		t.Fatalf("cmd = %#v, want %#v", cmd, want)
 	}
diff --git a/backend/internal/adapters/agent/qwen/qwen.go b/backend/internal/adapters/agent/qwen/qwen.go
index 0ceb90681..68c1414d6 100644
--- a/backend/internal/adapters/agent/qwen/qwen.go
+++ b/backend/internal/adapters/agent/qwen/qwen.go
@@ -122,6 +122,9 @@ func (p *Plugin) GetRestoreCommand(ctx context.Context, cfg ports.RestoreConfig)
 	cmd = make([]string, 0, 6)
 	cmd = append(cmd, binary)
 	appendApprovalFlags(&cmd, cfg.Permissions)
+	if cfg.SystemPrompt != "" {
+		cmd = append(cmd, "--append-system-prompt", cfg.SystemPrompt)
+	}
 	cmd = append(cmd, "-r", agentSessionID)
 	return cmd, true, nil
 }
diff --git a/backend/internal/adapters/agent/qwen/qwen_test.go b/backend/internal/adapters/agent/qwen/qwen_test.go
index 034cfc054..17daad1a4 100644
--- a/backend/internal/adapters/agent/qwen/qwen_test.go
+++ b/backend/internal/adapters/agent/qwen/qwen_test.go
@@ -271,7 +271,8 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	plugin := &Plugin{resolvedBinary: "qwen"}
 
 	cmd, ok, err := plugin.GetRestoreCommand(context.Background(), ports.RestoreConfig{
-		Permissions: ports.PermissionModeAuto,
+		Permissions:  ports.PermissionModeAuto,
+		SystemPrompt: "restore instructions",
 		Session: ports.SessionRef{
 			Metadata: map[string]string{ports.MetadataKeyAgentSessionID: "sess-123"},
 		},
@@ -285,6 +286,7 @@ func TestGetRestoreCommandReadsAgentSessionID(t *testing.T) {
 	want := []string{
 		"qwen",
 		"--approval-mode", "auto",
+		"--append-system-prompt", "restore instructions",
 		"-r", "sess-123",
 	}
 	if !reflect.DeepEqual(cmd, want) {