diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index 99dde77f2..d67e2f965 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -3728,6 +3728,7 @@ func (b *LocalBackend) initPeerAPIListener() {
 		taildrop: taildrop.ManagerOptions{
 			Logf:             b.logf,
 			Clock:            tstime.DefaultClock{Clock: b.clock},
+			State:            b.store,
 			Dir:              fileRoot,
 			DirectFileMode:   b.directFileRoot != "",
 			AvoidFinalRename: !b.directFileDoFinalRename,
diff --git a/ipn/store.go b/ipn/store.go
index 3bef012ba..84ae00dd2 100644
--- a/ipn/store.go
+++ b/ipn/store.go
@@ -53,6 +53,11 @@
 	// CurrentProfileStateKey is the key under which we store the current
 	// profile.
 	CurrentProfileStateKey = StateKey("_current-profile")
+
+	// TaildropReceivedKey is the key to indicate whether any taildrop file
+	// has ever been received (even if partially).
+	// Any non-empty value indicates that at least one file has been received.
+	TaildropReceivedKey = StateKey("_taildrop-received")
 )
 
 // CurrentProfileID returns the StateKey that stores the
diff --git a/taildrop/delete.go b/taildrop/delete.go
index 12b95c020..aaef34df1 100644
--- a/taildrop/delete.go
+++ b/taildrop/delete.go
@@ -13,6 +13,7 @@
 	"sync"
 	"time"
 
+	"tailscale.com/ipn"
 	"tailscale.com/syncs"
 	"tailscale.com/tstime"
 	"tailscale.com/types/logger"
@@ -52,13 +53,24 @@ func (d *fileDeleter) Init(m *Manager, eventHook func(string)) {
 	d.dir = m.opts.Dir
 	d.event = eventHook
 
-	// From a cold-start, load the list of partial and deleted files.
 	d.byName = make(map[string]*list.Element)
 	d.emptySignal = make(chan struct{})
 	d.shutdownCtx, d.shutdown = context.WithCancel(context.Background())
+
+	// From a cold-start, load the list of partial and deleted files.
+	//
+	// Only run this if we have ever received at least one file
+	// to avoid ever touching the taildrop directory on systems (e.g., MacOS)
+	// that pop up a security dialog window upon first access.
+	if m.opts.State == nil {
+		return
+	}
+	if b, _ := m.opts.State.ReadState(ipn.TaildropReceivedKey); len(b) == 0 {
+		return
+	}
 	d.group.Go(func() {
-		d.event("start init")
-		defer d.event("end init")
+		d.event("start full-scan")
+		defer d.event("end full-scan")
 		rangeDir(d.dir, func(de fs.DirEntry) bool {
 			switch {
 			case d.shutdownCtx.Err() != nil:
diff --git a/taildrop/delete_test.go b/taildrop/delete_test.go
index 9066c7bc8..5fa4b9c37 100644
--- a/taildrop/delete_test.go
+++ b/taildrop/delete_test.go
@@ -11,6 +11,8 @@
 	"time"
 
 	"github.com/google/go-cmp/cmp"
+	"tailscale.com/ipn"
+	"tailscale.com/ipn/store/mem"
 	"tailscale.com/tstest"
 	"tailscale.com/tstime"
 	"tailscale.com/util/must"
@@ -72,6 +74,8 @@ func TestDeleter(t *testing.T) {
 	m.opts.Logf = t.Logf
 	m.opts.Clock = tstime.DefaultClock{Clock: clock}
 	m.opts.Dir = dir
+	m.opts.State = must.Get(mem.New(nil, ""))
+	must.Do(m.opts.State.WriteState(ipn.TaildropReceivedKey, []byte{1}))
 	fd.Init(&m, eventHook)
 	defer fd.Shutdown()
 	insert := func(name string) {
@@ -85,8 +89,8 @@ func TestDeleter(t *testing.T) {
 		fd.Remove(name)
 	}
 
-	checkEvents("start init")
-	checkEvents("end init", "start waitAndDelete")
+	checkEvents("start full-scan")
+	checkEvents("end full-scan", "start waitAndDelete")
 	checkDirectory("foo.partial", "bar.partial", "buzz.deleted")
 
 	advance(deleteDelay / 2)
@@ -134,3 +138,15 @@ func TestDeleter(t *testing.T) {
 	remove("wuzz.partial")
 	checkEvents("end waitAndDelete")
 }
+
+// Test that the asynchronous full scan of the taildrop directory does not occur
+// on a cold start if taildrop has never received any files.
+func TestDeleterInitWithoutTaildrop(t *testing.T) {
+	var m Manager
+	var fd fileDeleter
+	m.opts.Logf = t.Logf
+	m.opts.Dir = t.TempDir()
+	m.opts.State = must.Get(mem.New(nil, ""))
+	fd.Init(&m, func(event string) { t.Errorf("unexpected event: %v", event) })
+	fd.Shutdown()
+}
diff --git a/taildrop/send.go b/taildrop/send.go
index 42c223737..d96c3542c 100644
--- a/taildrop/send.go
+++ b/taildrop/send.go
@@ -13,6 +13,7 @@
 	"time"
 
 	"tailscale.com/envknob"
+	"tailscale.com/ipn"
 	"tailscale.com/tstime"
 	"tailscale.com/version/distro"
 )
@@ -136,6 +137,17 @@ func (m *Manager) PutFile(id ClientID, baseName string, r io.Reader, offset, len
 	}()
 	inFile.w = f
 
+	// Record that we have started to receive at least one file.
+	// This is used by the deleter upon a cold-start to scan the directory
+	// for any files that need to be deleted.
+	if m.opts.State != nil {
+		if b, _ := m.opts.State.ReadState(ipn.TaildropReceivedKey); len(b) == 0 {
+			if err := m.opts.State.WriteState(ipn.TaildropReceivedKey, []byte{1}); err != nil {
+				m.opts.Logf("WriteState error: %v", err) // non-fatal error
+			}
+		}
+	}
+
 	// A positive offset implies that we are resuming an existing file.
 	// Seek to the appropriate offset and truncate the file.
 	if offset != 0 {
diff --git a/taildrop/taildrop.go b/taildrop/taildrop.go
index ceda9cd39..39ab5aff5 100644
--- a/taildrop/taildrop.go
+++ b/taildrop/taildrop.go
@@ -67,8 +67,9 @@ func (id ClientID) partialSuffix() string {
 
 // ManagerOptions are options to configure the [Manager].
 type ManagerOptions struct {
-	Logf  logger.Logf
-	Clock tstime.DefaultClock
+	Logf  logger.Logf         // may be nil
+	Clock tstime.DefaultClock // may be nil
+	State ipn.StateStore      // may be nil
 
 	// Dir is the directory to store received files.
 	// This main either be the final location for the files