diff --git a/changelog/29176.txt b/changelog/29176.txt
new file mode 100644
index 0000000000..a701cd1170
--- /dev/null
+++ b/changelog/29176.txt
@@ -0,0 +1,3 @@
+```release-note:bug
+core: Prevent integer overflows of the barrier key counter on key rotation requests
+```
diff --git a/vault/barrier_aes_gcm.go b/vault/barrier_aes_gcm.go
index 1144c7e60f..e75b7a78a8 100644
--- a/vault/barrier_aes_gcm.go
+++ b/vault/barrier_aes_gcm.go
@@ -621,6 +621,11 @@ func (b *AESGCMBarrier) Rotate(ctx context.Context, randomSource io.Reader) (uin
 	term := b.keyring.ActiveTerm()
 	newTerm := term + 1
 
+	if newTerm < term {
+		// We've rolled over the uint32, don't allow this
+		return 0, errors.New("failed to generate a new term value due to integer overflow")
+	}
+
 	// Add a new encryption key
 	newKeyring, err := b.keyring.AddKey(&Key{
 		Term:    newTerm,
diff --git a/vault/barrier_aes_gcm_test.go b/vault/barrier_aes_gcm_test.go
index 1268bf006c..77c5fee7e0 100644
--- a/vault/barrier_aes_gcm_test.go
+++ b/vault/barrier_aes_gcm_test.go
@@ -8,6 +8,8 @@ import (
 	"context"
 	"crypto/rand"
 	"encoding/json"
+	"math"
+	"strings"
 	"testing"
 	"time"
 
@@ -697,6 +699,45 @@ func TestBarrier_LegacyRotate(t *testing.T) {
 	}
 }
 
+// TestBarrier_RotateFailsOnOverflow validates that if we ever actually hit the
+// barrier key rotation limit, we fail the rotation with an error.
+func TestBarrier_RotateFailsOnOverflow(t *testing.T) {
+	inm, err := inmem.NewInmem(nil, logger)
+	if err != nil {
+		t.Fatalf("err: %v", err)
+	}
+	b, err := NewAESGCMBarrier(inm, false)
+	if err != nil {
+		t.Fatalf("err: %v", err)
+	}
+	key, err := b.GenerateKey(rand.Reader)
+	if err != nil {
+		t.Fatalf("err: %v", err)
+	}
+
+	// Initialize the barrier
+	ctx := context.Background()
+	err = b.Initialize(ctx, key, nil, rand.Reader)
+	if err != nil {
+		t.Fatalf("err: %v", err)
+	}
+	err = b.Unseal(ctx, key)
+	if err != nil {
+		t.Fatalf("err: %v", err)
+	}
+
+	// Hack to avoid generating a lot of keys...
+	b.keyring.activeTerm = math.MaxUint32
+
+	_, err = b.Rotate(ctx, rand.Reader)
+	if err == nil {
+		t.Fatalf("Rotate should fail on overflow but did not")
+	}
+	if !strings.Contains(err.Error(), "integer overflow") {
+		t.Fatalf("Rotate failed but not for the expected reason of integer overflow: %v", err)
+	}
+}
+
 // TestBarrier_persistKeyring_Context checks that we get the right errors if
 // the context is cancelled or times-out before the first part of persistKeyring
 // is able to persist the keyring itself (i.e. we don't go on to try and persist