diff --git a/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter.go b/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter.go
index dae954906..0e4c52ed2 100644
--- a/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter.go
+++ b/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter.go
@@ -164,6 +164,18 @@ type Adapter struct {
 	mu     sync.RWMutex
 	closed bool
 
+	// promptGate is a 1-slot semaphore that serializes session/prompt calls so
+	// at most one is in flight against the bridge at a time. The ScheduleWakeup
+	// path injects a synthetic prompt via fireWakeup; without this gate it can
+	// race a user prompt, and the claude-agent-acp bridge then returns each
+	// prompt's stop_reason against the wrong turn — shifting chat turns one
+	// prompt behind. A queued synthetic prompt waits here and drains the wakeup
+	// turn once the in-flight prompt finishes. It is a channel rather than a
+	// sync.Mutex so the wait honours the caller's context (a wakeup whose
+	// timeout/lifetime context is cancelled while queued aborts instead of
+	// blocking on a stuck turn).
+	promptGate chan struct{}
+
 	// lifetimeCtx is cancelled by Close. Background work that may outlive
 	// the call site (e.g. the synthetic wakeup prompt goroutine) derives its
 	// context from this one so it aborts when the adapter shuts down rather
@@ -189,6 +201,7 @@ func NewAdapter(cfg *shared.Config, log *logger.Logger) *Adapter {
 		pendingWakeups:  make(map[string]*pendingWakeup),
 		usageBySession:  make(map[string]*usageTracker),
 		attachMgr:       shared.NewAttachmentManager(cfg.WorkDir, l.Zap()),
+		promptGate:      make(chan struct{}, 1),
 		lifetimeCtx:     ctx,
 		lifetimeCancel:  cancel,
 	}
diff --git a/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter_prompt.go b/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter_prompt.go
index 2528821bb..0bb4b5ce6 100644
--- a/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter_prompt.go
+++ b/apps/backend/internal/agentctl/server/adapter/transport/acp/adapter_prompt.go
@@ -16,16 +16,54 @@ import (
 // If pending context is set (from SetPendingContext), it will be prepended to the message.
 // Attachments (images) are converted to ACP ImageBlocks and included in the prompt.
 // When the prompt completes, a complete event is emitted via the updates channel.
+func (a *Adapter) Prompt(ctx context.Context, message string, attachments []v1.MessageAttachment) error {
+	// A user prompt always targets the current session, so it is not pinned.
+	return a.sendPrompt(ctx, message, attachments, "")
+}
+
+// sendPrompt serializes session/prompt calls through promptGate and sends one
+// prompt to the agent. When expectSession is non-empty the prompt is pinned to
+// that session: if the adapter's active session changed (or the adapter closed)
+// while this call waited on the gate, the prompt is dropped instead of being
+// sent to whatever session is now current. This is the ScheduleWakeup path —
+// a wakeup must reach the session it was scheduled for or not at all.
 //
 //nolint:cyclop,funlen // pre-existing complexity preserved from adapter.go file split
-func (a *Adapter) Prompt(ctx context.Context, message string, attachments []v1.MessageAttachment) error {
+func (a *Adapter) sendPrompt(ctx context.Context, message string, attachments []v1.MessageAttachment, expectSession string) error {
+	// Acquire the prompt gate, honouring ctx so a queued wakeup whose context
+	// is cancelled (timeout / adapter Close) aborts instead of blocking on a
+	// stuck in-flight turn.
+	select {
+	case a.promptGate <- struct{}{}:
+		defer func() { <-a.promptGate }()
+	case <-ctx.Done():
+		return ctx.Err()
+	}
+
 	a.mu.Lock()
 	conn := a.acpConn
 	sessionID := a.sessionID
-	pendingContext := a.pendingContext
-	a.pendingContext = "" // Clear after use
+	closed := a.closed
+	// A pinned prompt that no longer matches the active session (or a closed
+	// adapter) is dropped. Wakeup-pinned prompts are synthetic turns — they
+	// must not consume pendingContext reserved for the next user prompt (e.g.
+	// fork_session resume context).
+	drop := expectSession != "" && (closed || sessionID != expectSession)
+	var pendingContext string
+	if !drop && expectSession == "" {
+		pendingContext = a.pendingContext
+		a.pendingContext = "" // Clear after use
+	}
 	a.mu.Unlock()
 
+	if drop {
+		a.logger.Info("dropping queued wakeup prompt: session changed or adapter closed before it ran",
+			zap.String("scheduled_for", expectSession),
+			zap.String("current_session", sessionID),
+			zap.Bool("closed", closed))
+		return nil
+	}
+
 	if conn == nil {
 		return fmt.Errorf("adapter not initialized")
 	}
@@ -170,14 +208,15 @@ func (a *Adapter) Prompt(ctx context.Context, message string, attachments []v1.M
 // turn and emits visible ACP frames. The session must still match (the user
 // hasn't started a fresh session) and the adapter must not be closed.
 //
-// Concurrent-prompt safety: if a user prompt is already in flight when this
-// runs, both end up calling conn.Prompt() on the same ClientSideConnection.
-// That's safe at the wire level — the ACP SDK's Connection.sendMessage
-// holds a write mutex, so request frames never interleave on stdin, and
-// JSON-RPC pairs each response back to its originating request via id —
-// but it does mean two prompts can be in flight against the bridge at
-// once. The bridge serialises them in the order it receives them, which
-// is exactly what we want for a wakeup that races a user message.
+// Prompt serialization: the synthetic prompt goes through sendPrompt, which
+// gates on promptGate so only one session/prompt is in flight at a time. If a
+// user prompt is already running the wakeup waits behind it rather than racing
+// it — two concurrent conn.Prompt() calls would let the bridge return each
+// prompt's stop_reason against the wrong turn, shifting chat turns one prompt
+// behind. Because the wakeup can wait, the session is re-validated inside
+// sendPrompt (via the pinned expectSession argument): if a NewSession/LoadSession
+// changed the active session while the wakeup queued, it is dropped instead of
+// being injected into the new session.
 func (a *Adapter) fireWakeup(sessionID, prompt string) {
 	a.mu.RLock()
 	closed := a.closed
@@ -205,7 +244,9 @@ func (a *Adapter) fireWakeup(sessionID, prompt string) {
 		// prompt instead of letting it run against a dead subprocess.
 		ctx, cancel := context.WithTimeout(a.lifetimeCtx, wakeupPromptTimeout)
 		defer cancel()
-		if err := a.Prompt(ctx, prompt, nil); err != nil {
+		// Pin to the scheduled session: if the active session changed while this
+		// wakeup waited on the prompt gate, sendPrompt drops it.
+		if err := a.sendPrompt(ctx, prompt, nil, sessionID); err != nil {
 			a.logger.Error("synthetic wakeup prompt failed",
 				zap.String("session_id", sessionID),
 				zap.Error(err))
diff --git a/apps/backend/internal/agentctl/server/adapter/transport/acp/wakeup_concurrency_test.go b/apps/backend/internal/agentctl/server/adapter/transport/acp/wakeup_concurrency_test.go
new file mode 100644
index 000000000..77ef21f99
--- /dev/null
+++ b/apps/backend/internal/agentctl/server/adapter/transport/acp/wakeup_concurrency_test.go
@@ -0,0 +1,259 @@
+package acp
+
+import (
+	"context"
+	"io"
+	"sync"
+	"sync/atomic"
+	"testing"
+	"time"
+
+	"github.com/coder/acp-go-sdk"
+	"github.com/kandev/kandev/internal/agentctl/types/streams"
+)
+
+// concurrencyFakeAgent is a minimal acp.Agent whose Prompt handler blocks until
+// released, recording how many Prompt calls are in flight simultaneously. It
+// lets a test observe whether kandev issues two overlapping conn.Prompt() calls.
+type concurrencyFakeAgent struct {
+	entered     chan struct{} // one signal per Prompt entry
+	release     chan struct{} // closed to unblock all parked Prompts
+	inFlight    atomic.Int32
+	maxInFlight atomic.Int32
+}
+
+func (f *concurrencyFakeAgent) Prompt(_ context.Context, _ acp.PromptRequest) (acp.PromptResponse, error) {
+	cur := f.inFlight.Add(1)
+	for {
+		old := f.maxInFlight.Load()
+		if cur <= old || f.maxInFlight.CompareAndSwap(old, cur) {
+			break
+		}
+	}
+	f.entered <- struct{}{}
+	<-f.release
+	f.inFlight.Add(-1)
+	return acp.PromptResponse{StopReason: acp.StopReasonEndTurn}, nil
+}
+
+func (f *concurrencyFakeAgent) Initialize(_ context.Context, params acp.InitializeRequest) (acp.InitializeResponse, error) {
+	return acp.InitializeResponse{ProtocolVersion: params.ProtocolVersion}, nil
+}
+
+func (f *concurrencyFakeAgent) NewSession(_ context.Context, _ acp.NewSessionRequest) (acp.NewSessionResponse, error) {
+	return acp.NewSessionResponse{SessionId: "sess-concurrency-test"}, nil
+}
+
+func (f *concurrencyFakeAgent) Authenticate(_ context.Context, _ acp.AuthenticateRequest) (acp.AuthenticateResponse, error) {
+	return acp.AuthenticateResponse{}, nil
+}
+func (f *concurrencyFakeAgent) Cancel(_ context.Context, _ acp.CancelNotification) error { return nil }
+func (f *concurrencyFakeAgent) CloseSession(_ context.Context, _ acp.CloseSessionRequest) (acp.CloseSessionResponse, error) {
+	return acp.CloseSessionResponse{}, nil
+}
+func (f *concurrencyFakeAgent) ListSessions(_ context.Context, _ acp.ListSessionsRequest) (acp.ListSessionsResponse, error) {
+	return acp.ListSessionsResponse{}, nil
+}
+func (f *concurrencyFakeAgent) ResumeSession(_ context.Context, _ acp.ResumeSessionRequest) (acp.ResumeSessionResponse, error) {
+	return acp.ResumeSessionResponse{}, nil
+}
+func (f *concurrencyFakeAgent) SetSessionConfigOption(_ context.Context, _ acp.SetSessionConfigOptionRequest) (acp.SetSessionConfigOptionResponse, error) {
+	return acp.SetSessionConfigOptionResponse{}, nil
+}
+func (f *concurrencyFakeAgent) SetSessionMode(_ context.Context, _ acp.SetSessionModeRequest) (acp.SetSessionModeResponse, error) {
+	return acp.SetSessionModeResponse{}, nil
+}
+
+// setupConcurrencyFakeAgent wires an adapter to a blocking fake agent and
+// registers cleanup immediately so early t.Fatal paths cannot leak pipes or
+// background goroutines.
+func setupConcurrencyFakeAgent(t *testing.T) (*Adapter, *concurrencyFakeAgent) {
+	t.Helper()
+
+	a := newTestAdapter()
+	c2aR, c2aW := io.Pipe()
+	a2cR, a2cW := io.Pipe()
+	t.Cleanup(func() {
+		_ = a.Close()
+		_ = c2aW.Close()
+		_ = a2cW.Close()
+	})
+
+	if err := a.Connect(c2aW, a2cR); err != nil {
+		t.Fatalf("Connect: %v", err)
+	}
+
+	fa := &concurrencyFakeAgent{
+		entered: make(chan struct{}, 8),
+		release: make(chan struct{}),
+	}
+	_ = acp.NewAgentSideConnection(fa, a2cW, c2aR)
+	return a, fa
+}
+
+// waitForPromptComplete blocks until sendPrompt emits EventTypeComplete or times out.
+func waitForPromptComplete(t *testing.T, a *Adapter) {
+	t.Helper()
+	deadline := time.After(100 * time.Millisecond)
+	for {
+		select {
+		case ev := <-a.updatesCh:
+			if ev.Type == streams.EventTypeComplete {
+				return
+			}
+		case <-deadline:
+			t.Fatal("timed out waiting for prompt complete event")
+		}
+	}
+}
+
+// TestWakeupDoesNotRaceConcurrentPromptWithUserPrompt reproduces the
+// turn-misalignment bug: when a ScheduleWakeup timer fires while a user prompt
+// is still in flight, fireWakeup must NOT issue a second, concurrent
+// conn.Prompt() against the bridge. Two overlapping prompts are what desync the
+// bridge's per-prompt stop_reason from the turn it belongs to, shifting chat
+// turns one prompt behind.
+//
+// The fake agent blocks inside Prompt and records peak concurrency. Before this
+// fix, the synthetic wakeup prompt overlapped the user prompt (maxInFlight == 2)
+// because fireWakeup called conn.Prompt() concurrently. This test verifies the
+// fix serializes them so maxInFlight never exceeds 1 during the overlap window.
+func TestWakeupDoesNotRaceConcurrentPromptWithUserPrompt(t *testing.T) {
+	a, fa := setupConcurrencyFakeAgent(t)
+
+	ctx := context.Background()
+	if err := a.Initialize(ctx); err != nil {
+		t.Fatalf("Initialize: %v", err)
+	}
+	sid, err := a.NewSession(ctx, nil)
+	if err != nil {
+		t.Fatalf("NewSession: %v", err)
+	}
+
+	var userWG sync.WaitGroup
+	userWG.Add(1)
+	go func() {
+		defer userWG.Done()
+		_ = a.Prompt(ctx, "user message", nil)
+	}()
+
+	// Wait until the user prompt is parked inside the agent's Prompt handler.
+	select {
+	case <-fa.entered:
+	case <-time.After(5 * time.Second):
+		t.Fatal("user prompt never reached the agent")
+	}
+
+	// Fire the wakeup while the user prompt is still in flight.
+	a.fireWakeup(sid, "synthetic wakeup prompt")
+
+	// Wakeup must not enter the agent while the user prompt is still parked.
+	select {
+	case <-fa.entered:
+		t.Fatal("wakeup entered agent while user prompt was in flight")
+	case <-time.After(100 * time.Millisecond):
+	}
+
+	if fa.maxInFlight.Load() > 1 {
+		t.Fatalf("maxInFlight=%d during overlap window; prompts must be serialized so the bridge's stop_reason stays aligned with its turn", fa.maxInFlight.Load())
+	}
+
+	// Release the user prompt; the queued wakeup should run serially afterwards.
+	close(fa.release)
+	userWG.Wait()
+	waitForPromptComplete(t, a)
+
+	select {
+	case <-fa.entered:
+	case <-time.After(100 * time.Millisecond):
+		t.Fatal("wakeup never ran after user prompt completed")
+	}
+	waitForPromptComplete(t, a)
+}
+
+// TestWakeupDroppedWhenSessionChangesWhileQueued covers the case where a wakeup
+// prompt queues behind an in-flight user prompt and the adapter's active session
+// changes (NewSession/LoadSession/reset) before the wakeup gets the gate. The
+// queued wakeup must target the session it was scheduled for; if that session is
+// no longer current it must be dropped, not injected into the new session.
+func TestWakeupDroppedWhenSessionChangesWhileQueued(t *testing.T) {
+	a, fa := setupConcurrencyFakeAgent(t)
+
+	ctx := context.Background()
+	if err := a.Initialize(ctx); err != nil {
+		t.Fatalf("Initialize: %v", err)
+	}
+	origSession, err := a.NewSession(ctx, nil)
+	if err != nil {
+		t.Fatalf("NewSession: %v", err)
+	}
+
+	var userWG sync.WaitGroup
+	userWG.Add(1)
+	go func() {
+		defer userWG.Done()
+		_ = a.Prompt(ctx, "user message", nil)
+	}()
+	select {
+	case <-fa.entered:
+	case <-time.After(5 * time.Second):
+		t.Fatal("user prompt never reached the agent")
+	}
+
+	// Wakeup fires for the original session and queues behind the gate.
+	a.fireWakeup(origSession, "scheduled wakeup for original session")
+
+	// The active session changes while the wakeup waits (e.g. reset/resume).
+	a.mu.Lock()
+	a.sessionID = "different-session-after-reset"
+	a.mu.Unlock()
+
+	// Release the in-flight user prompt so the queued wakeup can run.
+	close(fa.release)
+	userWG.Wait()
+
+	select {
+	case <-fa.entered:
+		t.Fatal("queued wakeup was sent after the session changed; it must be dropped to avoid injecting into an unrelated session")
+	case <-time.After(100 * time.Millisecond):
+	}
+	waitForPromptComplete(t, a)
+}
+
+// TestWakeupDoesNotConsumePendingContext verifies that a synthetic wakeup prompt
+// does not read-and-clear pendingContext, which is reserved for the next user
+// prompt (e.g. fork_session resume context).
+func TestWakeupDoesNotConsumePendingContext(t *testing.T) {
+	a, fa := setupConcurrencyFakeAgent(t)
+
+	ctx := context.Background()
+	if err := a.Initialize(ctx); err != nil {
+		t.Fatalf("Initialize: %v", err)
+	}
+	sid, err := a.NewSession(ctx, nil)
+	if err != nil {
+		t.Fatalf("NewSession: %v", err)
+	}
+
+	const canary = "resume-context-for-next-user-prompt"
+	a.mu.Lock()
+	a.pendingContext = canary
+	a.mu.Unlock()
+
+	a.fireWakeup(sid, "scheduled wakeup prompt")
+
+	select {
+	case <-fa.entered:
+	case <-time.After(100 * time.Millisecond):
+		t.Fatal("wakeup never reached the agent")
+	}
+	close(fa.release)
+	waitForPromptComplete(t, a)
+
+	a.mu.Lock()
+	got := a.pendingContext
+	a.mu.Unlock()
+	if got != canary {
+		t.Fatalf("pendingContext=%q, want %q — wakeup must not consume resume context", got, canary)
+	}
+}