diff --git a/cmd/tailscaled/depaware.txt b/cmd/tailscaled/depaware.txt
index 387b944c1..7c4885a4b 100644
--- a/cmd/tailscaled/depaware.txt
+++ b/cmd/tailscaled/depaware.txt
@@ -474,7 +474,7 @@ tailscale.com/cmd/tailscaled dependencies: (generated by github.com/tailscale/de
         golang.org/x/crypto/internal/alias                           from golang.org/x/crypto/chacha20+
         golang.org/x/crypto/internal/poly1305                        from golang.org/x/crypto/chacha20poly1305+
         golang.org/x/crypto/nacl/box                                 from tailscale.com/types/key
-        golang.org/x/crypto/nacl/secretbox                           from golang.org/x/crypto/nacl/box
+        golang.org/x/crypto/nacl/secretbox                           from golang.org/x/crypto/nacl/box+
         golang.org/x/crypto/poly1305                                 from github.com/tailscale/wireguard-go/device
         golang.org/x/crypto/salsa20/salsa                            from golang.org/x/crypto/nacl/box+
   LD    golang.org/x/crypto/ssh                                      from github.com/pkg/sftp+
diff --git a/feature/tpm/tpm.go b/feature/tpm/tpm.go
index 18e56ae89..6feac85e3 100644
--- a/feature/tpm/tpm.go
+++ b/feature/tpm/tpm.go
@@ -5,14 +5,29 @@
 package tpm
 
 import (
+	"bytes"
+	"crypto/rand"
+	"encoding/json"
+	"errors"
+	"fmt"
+	"log"
+	"os"
+	"path/filepath"
 	"slices"
+	"strings"
 	"sync"
 
 	"github.com/google/go-tpm/tpm2"
 	"github.com/google/go-tpm/tpm2/transport"
+	"golang.org/x/crypto/nacl/secretbox"
+	"tailscale.com/atomicfile"
 	"tailscale.com/feature"
 	"tailscale.com/hostinfo"
+	"tailscale.com/ipn"
+	"tailscale.com/ipn/store"
+	"tailscale.com/paths"
 	"tailscale.com/tailcfg"
+	"tailscale.com/types/logger"
 )
 
 var infoOnce = sync.OnceValue(info)
@@ -22,10 +37,16 @@ func init() {
 	hostinfo.RegisterHostinfoNewHook(func(hi *tailcfg.Hostinfo) {
 		hi.TPM = infoOnce()
 	})
+	store.Register(storePrefix, newStore)
 }
 
-//lint:ignore U1000 used in Linux and Windows builds only
-func infoFromCapabilities(tpm transport.TPM) *tailcfg.TPMInfo {
+func info() *tailcfg.TPMInfo {
+	tpm, err := open()
+	if err != nil {
+		return nil
+	}
+	defer tpm.Close()
+
 	info := new(tailcfg.TPMInfo)
 	toStr := func(s *string) func(*tailcfg.TPMInfo, uint32) {
 		return func(info *tailcfg.TPMInfo, value uint32) {
@@ -81,3 +102,300 @@ func propToString(v uint32) string {
 	// Delete any non-printable ASCII characters.
 	return string(slices.DeleteFunc(chars, func(b byte) bool { return b < ' ' || b > '~' }))
 }
+
+const storePrefix = "tpmseal:"
+
+func newStore(logf logger.Logf, path string) (ipn.StateStore, error) {
+	path = strings.TrimPrefix(path, storePrefix)
+	if err := paths.MkStateDir(filepath.Dir(path)); err != nil {
+		return nil, fmt.Errorf("creating state directory: %w", err)
+	}
+	var parsed map[ipn.StateKey][]byte
+	bs, err := os.ReadFile(path)
+	if err != nil {
+		if !os.IsNotExist(err) {
+			return nil, fmt.Errorf("failed to open %q: %w", path, err)
+		}
+		logf("tpm.newStore: initializing state file")
+
+		var key [32]byte
+		// crypto/rand.Read never returns an error.
+		rand.Read(key[:])
+
+		store := &tpmStore{
+			logf:  logf,
+			path:  path,
+			key:   key,
+			cache: make(map[ipn.StateKey][]byte),
+		}
+		if err := store.writeSealed(); err != nil {
+			return nil, fmt.Errorf("failed to write initial state file: %w", err)
+		}
+		return store, nil
+	}
+
+	// State file exists, unseal and parse it.
+	var sealed encryptedData
+	if err := json.Unmarshal(bs, &sealed); err != nil {
+		return nil, fmt.Errorf("failed to unmarshal state file: %w", err)
+	}
+	if len(sealed.Data) == 0 || sealed.Key == nil || len(sealed.Nonce) == 0 {
+		return nil, fmt.Errorf("state file %q has not been TPM-sealed or is corrupt", path)
+	}
+	data, err := unseal(logf, sealed)
+	if err != nil {
+		return nil, fmt.Errorf("failed to unseal state file: %w", err)
+	}
+	if err := json.Unmarshal(data.Data, &parsed); err != nil {
+		return nil, fmt.Errorf("failed to parse state file: %w", err)
+	}
+	return &tpmStore{
+		logf:  logf,
+		path:  path,
+		key:   data.Key,
+		cache: parsed,
+	}, nil
+}
+
+// tpmStore is an ipn.StateStore that stores the state in a secretbox-encrypted
+// file using a TPM-sealed symmetric key.
+type tpmStore struct {
+	logf logger.Logf
+	path string
+	key  [32]byte
+
+	mu    sync.RWMutex
+	cache map[ipn.StateKey][]byte
+}
+
+func (s *tpmStore) ReadState(k ipn.StateKey) ([]byte, error) {
+	s.mu.RLock()
+	defer s.mu.RUnlock()
+	v, ok := s.cache[k]
+	if !ok {
+		return nil, ipn.ErrStateNotExist
+	}
+	return bytes.Clone(v), nil
+}
+
+func (s *tpmStore) WriteState(k ipn.StateKey, bs []byte) error {
+	s.mu.Lock()
+	defer s.mu.Unlock()
+	if bytes.Equal(s.cache[k], bs) {
+		return nil
+	}
+	s.cache[k] = bytes.Clone(bs)
+
+	return s.writeSealed()
+}
+
+func (s *tpmStore) writeSealed() error {
+	bs, err := json.Marshal(s.cache)
+	if err != nil {
+		return err
+	}
+	sealed, err := seal(s.logf, decryptedData{Key: s.key, Data: bs})
+	if err != nil {
+		return fmt.Errorf("failed to seal state file: %w", err)
+	}
+	buf, err := json.Marshal(sealed)
+	if err != nil {
+		return err
+	}
+	return atomicfile.WriteFile(s.path, buf, 0600)
+}
+
+// The nested levels of encoding and encryption are confusing, so here's what's
+// going on in plain English.
+//
+// Not all TPM devices support symmetric encryption (TPM2_EncryptDecrypt2)
+// natively, but they do support "sealing" small values (see
+// tpmSeal/tpmUnseal). The size limit is too small for the actual state file,
+// so we seal a symmetric key instead. This symmetric key is then used to seal
+// the actual data using nacl/secretbox.
+// Confusingly, both TPMs and secretbox use "seal" terminology.
+//
+// tpmSeal/tpmUnseal do the lower-level sealing of small []byte blobs, which we
+// use to seal a 32-byte secretbox key.
+//
+// seal/unseal do the higher-level sealing of store data using secretbox, and
+// also sealing of the symmetric key using TPM.
+
+// decryptedData contains the fully decrypted raw data along with the symmetric
+// key used for secretbox. This struct should only live in memory and never get
+// stored to disk!
+type decryptedData struct {
+	Key  [32]byte
+	Data []byte
+}
+
+func (decryptedData) MarshalJSON() ([]byte, error) {
+	return nil, errors.New("[unexpected]: decryptedData should never get JSON-marshaled!")
+}
+
+// encryptedData contains the secretbox-sealed data and nonce, along with a
+// TPM-sealed key. All fields are required.
+type encryptedData struct {
+	Key   *tpmSealedData `json:"key"`
+	Nonce []byte         `json:"nonce"`
+	Data  []byte         `json:"data"`
+}
+
+func seal(logf logger.Logf, dec decryptedData) (*encryptedData, error) {
+	var nonce [24]byte
+	// crypto/rand.Read never returns an error.
+	rand.Read(nonce[:])
+
+	sealedData := secretbox.Seal(nil, dec.Data, &nonce, &dec.Key)
+	sealedKey, err := tpmSeal(logf, dec.Key[:])
+	if err != nil {
+		return nil, fmt.Errorf("failed to seal encryption key to TPM: %w", err)
+	}
+
+	return &encryptedData{
+		Key:   sealedKey,
+		Nonce: nonce[:],
+		Data:  sealedData,
+	}, nil
+}
+
+func unseal(logf logger.Logf, data encryptedData) (*decryptedData, error) {
+	if len(data.Nonce) != 24 {
+		return nil, fmt.Errorf("nonce should be 24 bytes long, got %d", len(data.Nonce))
+	}
+
+	unsealedKey, err := tpmUnseal(logf, data.Key)
+	if err != nil {
+		return nil, fmt.Errorf("failed to unseal encryption key with TPM: %w", err)
+	}
+	if len(unsealedKey) != 32 {
+		return nil, fmt.Errorf("unsealed key should be 32 bytes long, got %d", len(unsealedKey))
+	}
+	unsealedData, ok := secretbox.Open(nil, data.Data, (*[24]byte)(data.Nonce), (*[32]byte)(unsealedKey))
+	if !ok {
+		return nil, errors.New("failed to unseal data")
+	}
+
+	return &decryptedData{
+		Key:  *(*[32]byte)(unsealedKey),
+		Data: unsealedData,
+	}, nil
+}
+
+type tpmSealedData struct {
+	Private []byte
+	Public  []byte
+}
+
+// withSRK runs fn with the loaded Storage Root Key (SRK) handle. The SRK is
+// flushed after fn returns.
+func withSRK(logf logger.Logf, tpm transport.TPM, fn func(srk tpm2.AuthHandle) error) error {
+	srkCmd := tpm2.CreatePrimary{
+		PrimaryHandle: tpm2.TPMRHOwner,
+		InPublic:      tpm2.New2B(tpm2.ECCSRKTemplate),
+	}
+	srkRes, err := srkCmd.Execute(tpm)
+	if err != nil {
+		return fmt.Errorf("tpm2.CreatePrimary: %w", err)
+	}
+	defer func() {
+		cmd := tpm2.FlushContext{FlushHandle: srkRes.ObjectHandle}
+		if _, err := cmd.Execute(tpm); err != nil {
+			logf("tpm2.FlushContext: failed to flush SRK handle: %v", err)
+		}
+	}()
+
+	return fn(tpm2.AuthHandle{
+		Handle: srkRes.ObjectHandle,
+		Name:   srkRes.Name,
+		Auth:   tpm2.HMAC(tpm2.TPMAlgSHA256, 32),
+	})
+}
+
+// tpmSeal seals the data using SRK of the local TPM.
+func tpmSeal(logf logger.Logf, data []byte) (*tpmSealedData, error) {
+	tpm, err := open()
+	if err != nil {
+		return nil, fmt.Errorf("opening TPM: %w", err)
+	}
+	defer tpm.Close()
+
+	var res *tpmSealedData
+	err = withSRK(logf, tpm, func(srk tpm2.AuthHandle) error {
+		sealCmd := tpm2.Create{
+			ParentHandle: srk,
+			InSensitive: tpm2.TPM2BSensitiveCreate{
+				Sensitive: &tpm2.TPMSSensitiveCreate{
+					Data: tpm2.NewTPMUSensitiveCreate(&tpm2.TPM2BSensitiveData{
+						Buffer: data,
+					}),
+				},
+			},
+			InPublic: tpm2.New2B(tpm2.TPMTPublic{
+				Type:    tpm2.TPMAlgKeyedHash,
+				NameAlg: tpm2.TPMAlgSHA256,
+				ObjectAttributes: tpm2.TPMAObject{
+					FixedTPM:     true,
+					FixedParent:  true,
+					UserWithAuth: true,
+				},
+			}),
+		}
+		sealRes, err := sealCmd.Execute(tpm)
+		if err != nil {
+			return fmt.Errorf("tpm2.Create: %w", err)
+		}
+
+		res = &tpmSealedData{
+			Private: sealRes.OutPrivate.Buffer,
+			Public:  sealRes.OutPublic.Bytes(),
+		}
+		return nil
+	})
+	return res, err
+}
+
+// tpmUnseal unseals the data using SRK of the local TPM.
+func tpmUnseal(logf logger.Logf, data *tpmSealedData) ([]byte, error) {
+	tpm, err := open()
+	if err != nil {
+		return nil, fmt.Errorf("opening TPM: %w", err)
+	}
+	defer tpm.Close()
+
+	var res []byte
+	err = withSRK(logf, tpm, func(srk tpm2.AuthHandle) error {
+		// Load the sealed object into the TPM first under SRK.
+		loadCmd := tpm2.Load{
+			ParentHandle: srk,
+			InPrivate:    tpm2.TPM2BPrivate{Buffer: data.Private},
+			InPublic:     tpm2.BytesAs2B[tpm2.TPMTPublic](data.Public),
+		}
+		loadRes, err := loadCmd.Execute(tpm)
+		if err != nil {
+			return fmt.Errorf("tpm2.Load: %w", err)
+		}
+		defer func() {
+			cmd := tpm2.FlushContext{FlushHandle: loadRes.ObjectHandle}
+			if _, err := cmd.Execute(tpm); err != nil {
+				log.Printf("tpm2.FlushContext: failed to flush loaded sealed blob handle: %v", err)
+			}
+		}()
+
+		// Then unseal the object.
+		unsealCmd := tpm2.Unseal{
+			ItemHandle: tpm2.NamedHandle{
+				Handle: loadRes.ObjectHandle,
+				Name:   loadRes.Name,
+			},
+		}
+		unsealRes, err := unsealCmd.Execute(tpm)
+		if err != nil {
+			return fmt.Errorf("tpm2.Unseal: %w", err)
+		}
+		res = unsealRes.OutData.Buffer
+
+		return nil
+	})
+	return res, err
+}
diff --git a/feature/tpm/tpm_linux.go b/feature/tpm/tpm_linux.go
index a90c0e153..f2d0f1402 100644
--- a/feature/tpm/tpm_linux.go
+++ b/feature/tpm/tpm_linux.go
@@ -4,15 +4,10 @@
 package tpm
 
 import (
+	"github.com/google/go-tpm/tpm2/transport"
 	"github.com/google/go-tpm/tpm2/transport/linuxtpm"
-	"tailscale.com/tailcfg"
 )
 
-func info() *tailcfg.TPMInfo {
-	t, err := linuxtpm.Open("/dev/tpm0")
-	if err != nil {
-		return nil
-	}
-	defer t.Close()
-	return infoFromCapabilities(t)
+func open() (transport.TPMCloser, error) {
+	return linuxtpm.Open("/dev/tpm0")
 }
diff --git a/feature/tpm/tpm_other.go b/feature/tpm/tpm_other.go
index ba7c67621..108b2c057 100644
--- a/feature/tpm/tpm_other.go
+++ b/feature/tpm/tpm_other.go
@@ -5,8 +5,12 @@
 
 package tpm
 
-import "tailscale.com/tailcfg"
+import (
+	"errors"
 
-func info() *tailcfg.TPMInfo {
-	return nil
+	"github.com/google/go-tpm/tpm2/transport"
+)
+
+func open() (transport.TPMCloser, error) {
+	return nil, errors.New("TPM not supported on this platform")
 }
diff --git a/feature/tpm/tpm_test.go b/feature/tpm/tpm_test.go
index fc0fc178c..a022b69b2 100644
--- a/feature/tpm/tpm_test.go
+++ b/feature/tpm/tpm_test.go
@@ -3,7 +3,17 @@
 
 package tpm
 
-import "testing"
+import (
+	"bytes"
+	"crypto/rand"
+	"errors"
+	"path/filepath"
+	"strconv"
+	"testing"
+
+	"tailscale.com/ipn"
+	"tailscale.com/ipn/store"
+)
 
 func TestPropToString(t *testing.T) {
 	for prop, want := range map[uint32]string{
@@ -17,3 +27,156 @@ func TestPropToString(t *testing.T) {
 		}
 	}
 }
+
+func skipWithoutTPM(t testing.TB) {
+	tpm, err := open()
+	if err != nil {
+		t.Skip("TPM not available")
+	}
+	tpm.Close()
+}
+
+func TestSealUnseal(t *testing.T) {
+	skipWithoutTPM(t)
+
+	data := make([]byte, 100*1024)
+	rand.Read(data)
+	var key [32]byte
+	rand.Read(key[:])
+
+	sealed, err := seal(t.Logf, decryptedData{Key: key, Data: data})
+	if err != nil {
+		t.Fatalf("seal: %v", err)
+	}
+	if bytes.Contains(sealed.Data, data) {
+		t.Fatalf("sealed data %q contains original input %q", sealed.Data, data)
+	}
+
+	unsealed, err := unseal(t.Logf, *sealed)
+	if err != nil {
+		t.Fatalf("unseal: %v", err)
+	}
+	if !bytes.Equal(data, unsealed.Data) {
+		t.Errorf("got unsealed data: %q, want: %q", unsealed, data)
+	}
+	if key != unsealed.Key {
+		t.Errorf("got unsealed key: %q, want: %q", unsealed.Key, key)
+	}
+}
+
+func TestStore(t *testing.T) {
+	skipWithoutTPM(t)
+
+	path := storePrefix + filepath.Join(t.TempDir(), "state")
+	store, err := newStore(t.Logf, path)
+	if err != nil {
+		t.Fatal(err)
+	}
+
+	checkState := func(t *testing.T, store ipn.StateStore, k ipn.StateKey, want []byte) {
+		got, err := store.ReadState(k)
+		if err != nil {
+			t.Errorf("ReadState(%q): %v", k, err)
+		}
+		if !bytes.Equal(want, got) {
+			t.Errorf("ReadState(%q): got %q, want %q", k, got, want)
+		}
+	}
+
+	k1, k2 := ipn.StateKey("k1"), ipn.StateKey("k2")
+	v1, v2 := []byte("v1"), []byte("v2")
+
+	t.Run("read-non-existent-key", func(t *testing.T) {
+		_, err := store.ReadState(k1)
+		if !errors.Is(err, ipn.ErrStateNotExist) {
+			t.Errorf("ReadState succeeded, want %v", ipn.ErrStateNotExist)
+		}
+	})
+
+	t.Run("read-write-k1", func(t *testing.T) {
+		if err := store.WriteState(k1, v1); err != nil {
+			t.Errorf("WriteState(%q, %q): %v", k1, v1, err)
+		}
+		checkState(t, store, k1, v1)
+	})
+
+	t.Run("read-write-k2", func(t *testing.T) {
+		if err := store.WriteState(k2, v2); err != nil {
+			t.Errorf("WriteState(%q, %q): %v", k2, v2, err)
+		}
+		checkState(t, store, k2, v2)
+	})
+
+	t.Run("update-k2", func(t *testing.T) {
+		v2 = []byte("new v2")
+		if err := store.WriteState(k2, v2); err != nil {
+			t.Errorf("WriteState(%q, %q): %v", k2, v2, err)
+		}
+		checkState(t, store, k2, v2)
+	})
+
+	t.Run("reopen-store", func(t *testing.T) {
+		store, err := newStore(t.Logf, path)
+		if err != nil {
+			t.Fatal(err)
+		}
+		checkState(t, store, k1, v1)
+		checkState(t, store, k2, v2)
+	})
+}
+
+func BenchmarkStore(b *testing.B) {
+	skipWithoutTPM(b)
+	b.StopTimer()
+
+	stores := make(map[string]ipn.StateStore)
+	key := ipn.StateKey(b.Name())
+
+	// Set up tpmStore
+	tpmStore, err := newStore(b.Logf, filepath.Join(b.TempDir(), "tpm.store"))
+	if err != nil {
+		b.Fatal(err)
+	}
+	if err := tpmStore.WriteState(key, []byte("-1")); err != nil {
+		b.Fatal(err)
+	}
+	stores["tpmStore"] = tpmStore
+
+	// Set up FileStore
+	fileStore, err := store.NewFileStore(b.Logf, filepath.Join(b.TempDir(), "file.store"))
+	if err != nil {
+		b.Fatal(err)
+	}
+	if err := fileStore.WriteState(key, []byte("-1")); err != nil {
+		b.Fatal(err)
+	}
+	stores["fileStore"] = fileStore
+
+	b.StartTimer()
+
+	for name, store := range stores {
+		b.Run(name, func(b *testing.B) {
+			b.Run("write-noop", func(b *testing.B) {
+				for range b.N {
+					if err := store.WriteState(key, []byte("-1")); err != nil {
+						b.Fatal(err)
+					}
+				}
+			})
+			b.Run("write", func(b *testing.B) {
+				for i := range b.N {
+					if err := store.WriteState(key, []byte(strconv.Itoa(i))); err != nil {
+						b.Fatal(err)
+					}
+				}
+			})
+			b.Run("read", func(b *testing.B) {
+				for range b.N {
+					if _, err := store.ReadState(key); err != nil {
+						b.Fatal(err)
+					}
+				}
+			})
+		})
+	}
+}
diff --git a/feature/tpm/tpm_windows.go b/feature/tpm/tpm_windows.go
index 578d687af..429d20cb8 100644
--- a/feature/tpm/tpm_windows.go
+++ b/feature/tpm/tpm_windows.go
@@ -4,15 +4,10 @@
 package tpm
 
 import (
+	"github.com/google/go-tpm/tpm2/transport"
 	"github.com/google/go-tpm/tpm2/transport/windowstpm"
-	"tailscale.com/tailcfg"
 )
 
-func info() *tailcfg.TPMInfo {
-	t, err := windowstpm.Open()
-	if err != nil {
-		return nil
-	}
-	defer t.Close()
-	return infoFromCapabilities(t)
+func open() (transport.TPMCloser, error) {
+	return windowstpm.Open()
 }
diff --git a/ipn/store/stores.go b/ipn/store/stores.go
index 1f98891bf..1a98574c9 100644
--- a/ipn/store/stores.go
+++ b/ipn/store/stores.go
@@ -45,6 +45,8 @@ var knownStores map[string]Provider
 //     the suffix an AWS ARN for an SSM.
 //   - (Linux-only) if the string begins with "kube:",
 //     the suffix is a Kubernetes secret name
+//   - (Linux or Windows) if the string begins with "tpmseal:", the suffix is
+//     filepath that is sealed with the local TPM device.
 //   - In all other cases, the path is treated as a filepath.
 func New(logf logger.Logf, path string) (ipn.StateStore, error) {
 	for prefix, sf := range knownStores {