diff --git a/api/gen/proto/go/teleport/machineid/v1/bot_instance.pb.go b/api/gen/proto/go/teleport/machineid/v1/bot_instance.pb.go
index 8a6b2b25fdb72..c89535a11afc2 100644
--- a/api/gen/proto/go/teleport/machineid/v1/bot_instance.pb.go
+++ b/api/gen/proto/go/teleport/machineid/v1/bot_instance.pb.go
@@ -144,10 +144,6 @@ type BotInstanceSpec struct {
 	BotName string `protobuf:"bytes,1,opt,name=bot_name,json=botName,proto3" json:"bot_name,omitempty"`
 	// The unique identifier for this instance.
 	InstanceId string `protobuf:"bytes,2,opt,name=instance_id,json=instanceId,proto3" json:"instance_id,omitempty"`
-	// The desired expiration offset for this bot instance. The expiration will be
-	// calculated from the current time at creation or authentication plus this
-	// value. A nil `ttl` will not expire.
-	Ttl *durationpb.Duration `protobuf:"bytes,3,opt,name=ttl,proto3" json:"ttl,omitempty"`
 }
 
 func (x *BotInstanceSpec) Reset() {
@@ -196,13 +192,6 @@ func (x *BotInstanceSpec) GetInstanceId() string {
 	return ""
 }
 
-func (x *BotInstanceSpec) GetTtl() *durationpb.Duration {
-	if x != nil {
-		return x.Ttl
-	}
-	return nil
-}
-
 // BotInstanceStatusHeartbeat contains information self-reported by an instance
 // of a Bot. This information is not verified by the server and should not be
 // trusted.
@@ -354,8 +343,6 @@ type BotInstanceStatusAuthentication struct {
 	Generation int32 `protobuf:"varint,5,opt,name=generation,proto3" json:"generation,omitempty"`
 	// The public key of the Bot instance.
 	PublicKey []byte `protobuf:"bytes,6,opt,name=public_key,json=publicKey,proto3" json:"public_key,omitempty"`
-	// The fingerprint of the public key of the Bot instance.
-	Fingerprint string `protobuf:"bytes,7,opt,name=fingerprint,proto3" json:"fingerprint,omitempty"`
 }
 
 func (x *BotInstanceStatusAuthentication) Reset() {
@@ -432,13 +419,6 @@ func (x *BotInstanceStatusAuthentication) GetPublicKey() []byte {
 	return nil
 }
 
-func (x *BotInstanceStatusAuthentication) GetFingerprint() string {
-	if x != nil {
-		return x.Fingerprint
-	}
-	return ""
-}
-
 // BotInstanceStatus holds the status of a BotInstance.
 type BotInstanceStatus struct {
 	state         protoimpl.MessageState
@@ -547,89 +527,86 @@ var file_teleport_machineid_v1_bot_instance_proto_rawDesc = []byte{
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+	0x62, 0x06, 0x70, 0x72, 0x6f, 0x74, 0x6f, 0x33,
 }
 
 var (
@@ -652,28 +629,27 @@ var file_teleport_machineid_v1_bot_instance_proto_goTypes = []any{
 	(*BotInstanceStatusAuthentication)(nil), // 3: teleport.machineid.v1.BotInstanceStatusAuthentication
 	(*BotInstanceStatus)(nil),               // 4: teleport.machineid.v1.BotInstanceStatus
 	(*v1.Metadata)(nil),                     // 5: teleport.header.v1.Metadata
-	(*durationpb.Duration)(nil),             // 6: google.protobuf.Duration
-	(*timestamppb.Timestamp)(nil),           // 7: google.protobuf.Timestamp
+	(*timestamppb.Timestamp)(nil),           // 6: google.protobuf.Timestamp
+	(*durationpb.Duration)(nil),             // 7: google.protobuf.Duration
 	(*structpb.Struct)(nil),                 // 8: google.protobuf.Struct
 }
 var file_teleport_machineid_v1_bot_instance_proto_depIdxs = []int32{
 	5,  // 0: teleport.machineid.v1.BotInstance.metadata:type_name -> teleport.header.v1.Metadata
 	1,  // 1: teleport.machineid.v1.BotInstance.spec:type_name -> teleport.machineid.v1.BotInstanceSpec
 	4,  // 2: teleport.machineid.v1.BotInstance.status:type_name -> teleport.machineid.v1.BotInstanceStatus
-	6,  // 3: teleport.machineid.v1.BotInstanceSpec.ttl:type_name -> google.protobuf.Duration
-	7,  // 4: teleport.machineid.v1.BotInstanceStatusHeartbeat.recorded_at:type_name -> google.protobuf.Timestamp
-	6,  // 5: teleport.machineid.v1.BotInstanceStatusHeartbeat.uptime:type_name -> google.protobuf.Duration
-	7,  // 6: teleport.machineid.v1.BotInstanceStatusAuthentication.authenticated_at:type_name -> google.protobuf.Timestamp
-	8,  // 7: teleport.machineid.v1.BotInstanceStatusAuthentication.metadata:type_name -> google.protobuf.Struct
-	3,  // 8: teleport.machineid.v1.BotInstanceStatus.initial_authentication:type_name -> teleport.machineid.v1.BotInstanceStatusAuthentication
-	3,  // 9: teleport.machineid.v1.BotInstanceStatus.latest_authentications:type_name -> teleport.machineid.v1.BotInstanceStatusAuthentication
-	2,  // 10: teleport.machineid.v1.BotInstanceStatus.initial_heartbeat:type_name -> teleport.machineid.v1.BotInstanceStatusHeartbeat
-	2,  // 11: teleport.machineid.v1.BotInstanceStatus.latest_heartbeats:type_name -> teleport.machineid.v1.BotInstanceStatusHeartbeat
-	12, // [12:12] is the sub-list for method output_type
-	12, // [12:12] is the sub-list for method input_type
-	12, // [12:12] is the sub-list for extension type_name
-	12, // [12:12] is the sub-list for extension extendee
-	0,  // [0:12] is the sub-list for field type_name
+	6,  // 3: teleport.machineid.v1.BotInstanceStatusHeartbeat.recorded_at:type_name -> google.protobuf.Timestamp
+	7,  // 4: teleport.machineid.v1.BotInstanceStatusHeartbeat.uptime:type_name -> google.protobuf.Duration
+	6,  // 5: teleport.machineid.v1.BotInstanceStatusAuthentication.authenticated_at:type_name -> google.protobuf.Timestamp
+	8,  // 6: teleport.machineid.v1.BotInstanceStatusAuthentication.metadata:type_name -> google.protobuf.Struct
+	3,  // 7: teleport.machineid.v1.BotInstanceStatus.initial_authentication:type_name -> teleport.machineid.v1.BotInstanceStatusAuthentication
+	3,  // 8: teleport.machineid.v1.BotInstanceStatus.latest_authentications:type_name -> teleport.machineid.v1.BotInstanceStatusAuthentication
+	2,  // 9: teleport.machineid.v1.BotInstanceStatus.initial_heartbeat:type_name -> teleport.machineid.v1.BotInstanceStatusHeartbeat
+	2,  // 10: teleport.machineid.v1.BotInstanceStatus.latest_heartbeats:type_name -> teleport.machineid.v1.BotInstanceStatusHeartbeat
+	11, // [11:11] is the sub-list for method output_type
+	11, // [11:11] is the sub-list for method input_type
+	11, // [11:11] is the sub-list for extension type_name
+	11, // [11:11] is the sub-list for extension extendee
+	0,  // [0:11] is the sub-list for field type_name
 }
 
 func init() { file_teleport_machineid_v1_bot_instance_proto_init() }
diff --git a/api/proto/teleport/machineid/v1/bot_instance.proto b/api/proto/teleport/machineid/v1/bot_instance.proto
index 94ae95f82a757..bd231b4a0dac4 100644
--- a/api/proto/teleport/machineid/v1/bot_instance.proto
+++ b/api/proto/teleport/machineid/v1/bot_instance.proto
@@ -47,10 +47,9 @@ message BotInstanceSpec {
   string bot_name = 1;
   // The unique identifier for this instance.
   string instance_id = 2;
-  // The desired expiration offset for this bot instance. The expiration will be
-  // calculated from the current time at creation or authentication plus this
-  // value. A nil `ttl` will not expire.
-  google.protobuf.Duration ttl = 3;
+
+  reserved 3;
+  reserved "ttl";
 }
 
 // BotInstanceStatusHeartbeat contains information self-reported by an instance
@@ -104,8 +103,9 @@ message BotInstanceStatusAuthentication {
   int32 generation = 5;
   // The public key of the Bot instance.
   bytes public_key = 6;
-  // The fingerprint of the public key of the Bot instance.
-  string fingerprint = 7;
+
+  reserved 7;
+  reserved "fingerprint";
 }
 
 // BotInstanceStatus holds the status of a BotInstance.
diff --git a/constants.go b/constants.go
index a1fec710bb8f1..7fa1cb7162119 100644
--- a/constants.go
+++ b/constants.go
@@ -503,6 +503,10 @@ const (
 	// CertExtensionBotName indicates the name of the Machine ID bot this
 	// certificate was issued to, if any.
 	CertExtensionBotName = "bot-name@goteleport.com"
+	// CertExtensionBotInstanceID indicates the unique identifier of this
+	// Machine ID bot instance, if any. This identifier is persisted through
+	// certificate renewals.
+	CertExtensionBotInstanceID = "bot-instance-id@goteleport.com"
 
 	// CertCriticalOptionSourceAddress is a critical option that defines IP addresses (in CIDR notation)
 	// from which this certificate is accepted for authentication.
diff --git a/lib/auth/auth.go b/lib/auth/auth.go
index d7581d6360cbf..a22291e973a02 100644
--- a/lib/auth/auth.go
+++ b/lib/auth/auth.go
@@ -2026,6 +2026,9 @@ type certRequest struct {
 	deviceExtensions DeviceExtensions
 	// botName is the name of the bot requesting this cert, if any
 	botName string
+	// botInstanceID is the unique identifier of the bot instance associated
+	// with this cert, if any
+	botInstanceID string
 }
 
 // check verifies the cert request is valid.
@@ -2969,6 +2972,7 @@ func generateCert(ctx context.Context, a *Server, req certRequest, caType types.
 		Renewable:               req.renewable,
 		Generation:              req.generation,
 		BotName:                 req.botName,
+		BotInstanceID:           req.botInstanceID,
 		CertificateExtensions:   req.checker.CertificateExtensions(),
 		AllowedResourceIDs:      requestedResourcesStr,
 		ConnectionDiagnosticID:  req.connectionDiagnosticID,
@@ -3064,6 +3068,7 @@ func generateCert(ctx context.Context, a *Server, req certRequest, caType types.
 		Renewable:               req.renewable,
 		Generation:              req.generation,
 		BotName:                 req.botName,
+		BotInstanceID:           req.botInstanceID,
 		AllowedResourceIDs:      req.checker.GetAllowedResourceIDs(),
 		PrivateKeyPolicy:        attestedKeyPolicy,
 		ConnectionDiagnosticID:  req.connectionDiagnosticID,
diff --git a/lib/auth/auth_with_roles.go b/lib/auth/auth_with_roles.go
index e6d8e2bf1110b..ee06363d4635a 100644
--- a/lib/auth/auth_with_roles.go
+++ b/lib/auth/auth_with_roles.go
@@ -3252,6 +3252,12 @@ func (a *ServerWithRoles) generateUserCerts(ctx context.Context, req proto.UserC
 		connectionDiagnosticID: req.ConnectionDiagnosticID,
 		attestationStatement:   keys.AttestationStatementFromProto(req.AttestationStatement),
 		botName:                getBotName(user),
+
+		// Always pass through a bot instance ID if available. Legacy bots
+		// joining without an instance ID may have one generated when
+		// `updateBotInstance()` is called below, and this (empty) value will be
+		// overridden.
+		botInstanceID: a.context.Identity.GetIdentity().BotInstanceID,
 	}
 	if user.GetName() != a.context.User.GetName() {
 		certReq.impersonator = a.context.User.GetName()
@@ -3304,6 +3310,12 @@ func (a *ServerWithRoles) generateUserCerts(ctx context.Context, req proto.UserC
 		if err := a.authServer.validateGenerationLabel(ctx, user.GetName(), &certReq, currentIdentityGeneration); err != nil {
 			return nil, trace.Wrap(err)
 		}
+
+		// Update the bot instance based on this authentication. This may create
+		// a new bot instance record if the identity is missing an instance ID.
+		if err := a.updateBotInstance(ctx, &certReq); err != nil {
+			return nil, trace.Wrap(err)
+		}
 	}
 
 	certs, err := a.authServer.generateUserCert(ctx, certReq)
diff --git a/lib/auth/bot.go b/lib/auth/bot.go
index 472d5f672e922..7ba9a746fdf62 100644
--- a/lib/auth/bot.go
+++ b/lib/auth/bot.go
@@ -26,11 +26,17 @@ import (
 
 	"github.com/google/uuid"
 	"github.com/gravitational/trace"
+	"github.com/sirupsen/logrus"
+	"google.golang.org/protobuf/types/known/timestamppb"
 
 	"github.com/gravitational/teleport/api/client/proto"
+	headerv1 "github.com/gravitational/teleport/api/gen/proto/go/teleport/header/v1"
+	machineidv1pb "github.com/gravitational/teleport/api/gen/proto/go/teleport/machineid/v1"
 	"github.com/gravitational/teleport/api/types"
 	apievents "github.com/gravitational/teleport/api/types/events"
 	apiutils "github.com/gravitational/teleport/api/utils"
+	"github.com/gravitational/teleport/lib/auth/machineid/machineidv1"
+	experiment "github.com/gravitational/teleport/lib/auth/machineid/machineidv1/bot_instance_experiment"
 	"github.com/gravitational/teleport/lib/authz"
 	"github.com/gravitational/teleport/lib/defaults"
 	"github.com/gravitational/teleport/lib/events"
@@ -168,6 +174,120 @@ func (a *Server) validateGenerationLabel(ctx context.Context, username string, c
 	return nil
 }
 
+// updateBotInstance updates the bot instance associated with the context
+// identity, if any.
+func (a *ServerWithRoles) updateBotInstance(ctx context.Context, req *certRequest) error {
+	ident := a.context.Identity.GetIdentity()
+
+	if !experiment.Enabled() {
+		// Only attempt to update bot instances if the experiment is enabled.
+		return nil
+	}
+
+	if ident.BotName == "" {
+		// Only applies to bot identities
+		return nil
+	}
+
+	authRecord := &machineidv1pb.BotInstanceStatusAuthentication{
+		AuthenticatedAt: timestamppb.New(a.authServer.GetClock().Now()),
+		PublicKey:       req.publicKey,
+
+		// TODO: for now, this copy of the certificate generation only is
+		// informational. Future changes will transition to trusting (and
+		// verifying) this value in lieu of the old generation label on bot
+		// users.
+		Generation: int32(req.generation),
+
+		// Note: This auth path can only ever be for token joins; all other join
+		// types effectively rejoin every renewal. Other fields will be unset
+		// (metadata, join token name, etc).
+		JoinMethod: string(types.JoinMethodToken),
+	}
+
+	// An empty bot instance most likely means a bot is rejoining after an
+	// upgrade, so a new bot instance should be generated.
+	if ident.BotInstanceID == "" {
+		log.WithFields(logrus.Fields{
+			"bot_name": ident.BotName,
+		}).Info("bot has no instance ID, a new instance will be generated")
+
+		instanceID, err := uuid.NewRandom()
+		if err != nil {
+			return trace.Wrap(err)
+		}
+
+		expires := a.authServer.GetClock().Now().Add(req.ttl + machineidv1.ExpiryMargin)
+
+		bi := newBotInstance(&machineidv1pb.BotInstanceSpec{
+			BotName:    ident.BotName,
+			InstanceId: instanceID.String(),
+		}, authRecord, expires)
+
+		if _, err := a.authServer.BotInstance.CreateBotInstance(ctx, bi); err != nil {
+			return trace.Wrap(err)
+		}
+
+		// Add the new ID to the cert request
+		req.botInstanceID = instanceID.String()
+
+		return nil
+	}
+
+	_, err := a.authServer.BotInstance.PatchBotInstance(ctx, ident.BotName, ident.BotInstanceID, func(bi *machineidv1pb.BotInstance) (*machineidv1pb.BotInstance, error) {
+		if bi.Status == nil {
+			bi.Status = &machineidv1pb.BotInstanceStatus{}
+		}
+
+		// Update the record's expiration timestamp based on the request TTL
+		// plus an expiry margin.
+		bi.Metadata.Expires = timestamppb.New(a.authServer.GetClock().Now().Add(req.ttl + machineidv1.ExpiryMargin))
+
+		// If we're at or above the limit, remove enough of the front elements
+		// to make room for the new one at the end.
+		if len(bi.Status.LatestAuthentications) >= machineidv1.AuthenticationHistoryLimit {
+			toRemove := len(bi.Status.LatestAuthentications) - machineidv1.AuthenticationHistoryLimit + 1
+			bi.Status.LatestAuthentications = bi.Status.LatestAuthentications[toRemove:]
+		}
+
+		// An initial auth record should have been added during initial join,
+		// but if not, add it now.
+		if bi.Status.InitialAuthentication == nil {
+			log.WithFields(logrus.Fields{
+				"bot_name":        ident.BotName,
+				"bot_instance_id": ident.BotInstanceID,
+			}).Warn("bot instance is missing its initial authentication record, a new one will be added")
+			bi.Status.InitialAuthentication = authRecord
+		}
+
+		bi.Status.LatestAuthentications = append(bi.Status.LatestAuthentications, authRecord)
+
+		return bi, nil
+	})
+
+	return trace.Wrap(err)
+}
+
+// newBotInstance constructs a new bot instance from a spec and initial authentication
+func newBotInstance(
+	spec *machineidv1pb.BotInstanceSpec,
+	initialAuth *machineidv1pb.BotInstanceStatusAuthentication,
+	expires time.Time,
+) *machineidv1pb.BotInstance {
+	return &machineidv1pb.BotInstance{
+		Kind:    types.KindBotInstance,
+		Version: types.V1,
+		Metadata: &headerv1.Metadata{
+			Expires: timestamppb.New(expires),
+		},
+		Spec: spec,
+		Status: &machineidv1pb.BotInstanceStatus{
+			InitialAuthentication: initialAuth,
+			LatestAuthentications: []*machineidv1pb.BotInstanceStatusAuthentication{initialAuth},
+		},
+	}
+}
+
 // generateInitialBotCerts is used to generate bot certs and overlaps
 // significantly with `generateUserCerts()`. However, it omits a number of
 // options (impersonation, access requests, role requests, actual cert renewal,
@@ -175,7 +295,10 @@ func (a *Server) validateGenerationLabel(ctx context.Context, username string, c
 // care if the current identity is Nop.  This function does not validate the
 // current identity at all; the caller is expected to validate that the client
 // is allowed to issue the (possibly renewable) certificates.
-func (a *Server) generateInitialBotCerts(ctx context.Context, botName, username, loginIP string, pubKey []byte, expires time.Time, renewable bool) (*proto.Certs, error) {
+func (a *Server) generateInitialBotCerts(
+	ctx context.Context, botName, username, loginIP string, pubKey []byte,
+	expires time.Time, renewable bool, initialAuth *machineidv1pb.BotInstanceStatusAuthentication,
+) (*proto.Certs, error) {
 	var err error
 
 	// Extract the user and role set for whom the certificate will be generated.
@@ -216,6 +339,27 @@ func (a *Server) generateInitialBotCerts(ctx context.Context, botName, username,
 	var generation uint64
 	if renewable {
 		generation = 1
+		initialAuth.Generation = 1
+	}
+
+	var botInstanceID string
+	if experiment.Enabled() {
+		uuid, err := uuid.NewRandom()
+		if err != nil {
+			return nil, trace.Wrap(err)
+		}
+
+		bi := newBotInstance(&machineidv1pb.BotInstanceSpec{
+			BotName:    botName,
+			InstanceId: uuid.String(),
+		}, initialAuth, expires.Add(machineidv1.ExpiryMargin))
+
+		_, err = a.BotInstance.CreateBotInstance(ctx, bi)
+		if err != nil {
+			return nil, trace.Wrap(err)
+		}
+
+		botInstanceID = uuid.String()
 	}
 
 	// Generate certificate
@@ -230,6 +374,7 @@ func (a *Server) generateInitialBotCerts(ctx context.Context, botName, username,
 		generation:    generation,
 		loginIP:       loginIP,
 		botName:       botName,
+		botInstanceID: botInstanceID,
 	}
 
 	if err := a.validateGenerationLabel(ctx, userState.GetName(), &certReq, 0); err != nil {
diff --git a/lib/auth/bot_test.go b/lib/auth/bot_test.go
index 4c54114a96522..e053a7cf8b860 100644
--- a/lib/auth/bot_test.go
+++ b/lib/auth/bot_test.go
@@ -34,6 +34,7 @@ import (
 	"github.com/digitorus/pkcs7"
 	"github.com/google/uuid"
 	"github.com/gravitational/trace"
+	"github.com/jonboulle/clockwork"
 	"github.com/stretchr/testify/require"
 	"golang.org/x/crypto/ssh"
 
@@ -44,6 +45,7 @@ import (
 	"github.com/gravitational/teleport/lib/auth/authclient"
 	"github.com/gravitational/teleport/lib/auth/join"
 	"github.com/gravitational/teleport/lib/auth/machineid/machineidv1"
+	experiment "github.com/gravitational/teleport/lib/auth/machineid/machineidv1/bot_instance_experiment"
 	"github.com/gravitational/teleport/lib/auth/state"
 	"github.com/gravitational/teleport/lib/auth/testauthority"
 	"github.com/gravitational/teleport/lib/cloud/azure"
@@ -60,12 +62,13 @@ func renewBotCerts(
 	publicKey []byte,
 	privateKey []byte,
 ) (*authclient.Client, *proto.Certs, tls.Certificate, error) {
+	fakeClock := srv.Clock().(clockwork.FakeClock)
 	client := srv.NewClientWithCert(tlsCert)
 
 	certs, err := client.GenerateUserCerts(ctx, proto.UserCertsRequest{
 		PublicKey: publicKey,
 		Username:  botUser,
-		Expires:   time.Now().Add(time.Hour),
+		Expires:   fakeClock.Now().Add(time.Hour),
 	})
 	if err != nil {
 		return nil, nil, tls.Certificate{}, trace.Wrap(err)
@@ -83,9 +86,18 @@ func renewBotCerts(
 // TestRegisterBotCertificateGenerationCheck ensures bot cert generation checks
 // work in ordinary conditions, with several rapid renewals.
 func TestRegisterBotCertificateGenerationCheck(t *testing.T) {
-	t.Parallel()
+	// TODO: Enable parallel once the experiment is removed
+	//  t.Parallel()
+
+	experimentBefore := experiment.Enabled()
+	experiment.SetEnabled(true)
+	t.Cleanup(func() {
+		experiment.SetEnabled(experimentBefore)
+	})
+
 	srv := newTestTLSServer(t)
 	ctx := context.Background()
+	fakeClock := srv.Clock().(clockwork.FakeClock)
 
 	_, err := CreateRole(ctx, srv.Auth(), "example", types.RoleSpecV6{})
 	require.NoError(t, err)
@@ -131,29 +143,152 @@ func TestRegisterBotCertificateGenerationCheck(t *testing.T) {
 	require.NoError(t, err)
 	checkCertLoginIP(t, certs.TLS, "127.0.0.1")
 
+	initialCert, err := tlsca.ParseCertificatePEM(certs.TLS)
+	require.NoError(t, err)
+	initialIdent, err := tlsca.FromSubject(initialCert.Subject, initialCert.NotAfter)
+	require.NoError(t, err)
+
+	require.Equal(t, uint64(1), initialIdent.Generation)
+	require.Equal(t, "test", initialIdent.BotName)
+	require.NotEmpty(t, initialIdent.BotInstanceID)
+
 	tlsCert, err := tls.X509KeyPair(certs.TLS, privateKey)
 	require.NoError(t, err)
 
 	// Renew the cert a bunch of times.
 	for i := 0; i < 10; i++ {
+		// Ensure the state of the bot instance before renewal is sane.
+		bi, err := srv.Auth().BotInstance.GetBotInstance(ctx, initialIdent.BotName, initialIdent.BotInstanceID)
+		require.NoError(t, err)
+
+		// There should always be at least 1 entry as the initial join is
+		// duplicated in the list.
+		require.Len(t, bi.Status.LatestAuthentications, min(i+1, machineidv1.AuthenticationHistoryLimit))
+
+		// Generation starts at 1 for initial certs.
+		latest := bi.Status.LatestAuthentications[len(bi.Status.LatestAuthentications)-1]
+		require.Equal(t, int32(i+1), latest.Generation)
+
+		lastExpires := bi.Metadata.Expires.AsTime()
+
+		// Advance the clock a bit.
+		fakeClock.Advance(time.Minute)
+
 		_, certs, tlsCert, err = renewBotCerts(ctx, srv, tlsCert, bot.Status.UserName, publicKey, privateKey)
 		require.NoError(t, err)
 
 		// Parse the Identity
-		impersonatedTLSCert, err := tlsca.ParseCertificatePEM(certs.TLS)
+		renewedCert, err := tlsca.ParseCertificatePEM(certs.TLS)
 		require.NoError(t, err)
-		impersonatedIdent, err := tlsca.FromSubject(impersonatedTLSCert.Subject, impersonatedTLSCert.NotAfter)
+		renewedIdent, err := tlsca.FromSubject(renewedCert.Subject, renewedCert.NotAfter)
 		require.NoError(t, err)
 
 		// Cert must be renewable.
-		require.True(t, impersonatedIdent.Renewable)
-		require.False(t, impersonatedIdent.DisallowReissue)
+		require.True(t, renewedIdent.Renewable)
+		require.False(t, renewedIdent.DisallowReissue)
 
 		// Initial certs have generation=1 and we start the loop with a renewal, so add 2
-		require.Equal(t, uint64(i+2), impersonatedIdent.Generation)
+		require.Equal(t, uint64(i+2), renewedIdent.Generation)
+
+		// Ensure the bot instance after renewal is sane.
+		bi, err = srv.Auth().BotInstance.GetBotInstance(ctx, initialIdent.BotName, initialIdent.BotInstanceID)
+		require.NoError(t, err)
+
+		require.Len(t, bi.Status.LatestAuthentications, min(i+2, machineidv1.AuthenticationHistoryLimit))
+
+		latest = bi.Status.LatestAuthentications[len(bi.Status.LatestAuthentications)-1]
+		require.Equal(t, int32(i+2), latest.Generation)
+
+		require.True(t, bi.Metadata.Expires.AsTime().After(lastExpires), "Metadata.Expires must be extended")
 	}
 }
 
+// TestRegisterBotInstance tests that bot instances are created properly on join
+func TestRegisterBotInstance(t *testing.T) {
+	// TODO: Enable parallel once the experiment is removed
+	//  t.Parallel()
+
+	experimentBefore := experiment.Enabled()
+	experiment.SetEnabled(true)
+	t.Cleanup(func() {
+		experiment.SetEnabled(experimentBefore)
+	})
+
+	srv := newTestTLSServer(t)
+	ctx := context.Background()
+
+	_, err := CreateRole(ctx, srv.Auth(), "example", types.RoleSpecV6{})
+	require.NoError(t, err)
+
+	// Create a new bot.
+	client, err := srv.NewClient(TestAdmin())
+	require.NoError(t, err)
+	bot, err := client.BotServiceClient().CreateBot(ctx, &machineidv1pb.CreateBotRequest{
+		Bot: &machineidv1pb.Bot{
+			Metadata: &headerv1.Metadata{
+				Name: "test",
+			},
+			Spec: &machineidv1pb.BotSpec{
+				Roles: []string{"example"},
+			},
+		},
+	})
+	require.NoError(t, err)
+
+	token, err := types.NewProvisionTokenFromSpec("testxyzzy", time.Time{}, types.ProvisionTokenSpecV2{
+		Roles:   types.SystemRoles{types.RoleBot},
+		BotName: bot.Metadata.Name,
+	})
+	require.NoError(t, err)
+	require.NoError(t, client.CreateToken(ctx, token))
+
+	privateKey, publicKey, err := testauthority.New().GenerateKeyPair()
+	require.NoError(t, err)
+	sshPrivateKey, err := ssh.ParseRawPrivateKey(privateKey)
+	require.NoError(t, err)
+	tlsPublicKey, err := tlsca.MarshalPublicKeyFromPrivateKeyPEM(sshPrivateKey)
+	require.NoError(t, err)
+
+	certs, err := join.Register(ctx, join.RegisterParams{
+		Token: token.GetName(),
+		ID: state.IdentityID{
+			Role: types.RoleBot,
+		},
+		AuthServers:  []utils.NetAddr{*utils.MustParseAddr(srv.Addr().String())},
+		PublicTLSKey: tlsPublicKey,
+		PublicSSHKey: publicKey,
+	})
+	require.NoError(t, err)
+
+	// The returned certs should have a bot instance ID.
+	cert, err := tlsca.ParseCertificatePEM(certs.TLS)
+	require.NoError(t, err)
+
+	ident, err := tlsca.FromSubject(cert.Subject, cert.NotAfter)
+	require.NoError(t, err)
+
+	require.NotEmpty(t, ident.BotInstanceID)
+
+	// The instance ID should match a bot instance record.
+	botInstance, err := srv.Auth().BotInstance.GetBotInstance(ctx, ident.BotName, ident.BotInstanceID)
+	require.NoError(t, err)
+
+	require.Equal(t, ident.BotName, botInstance.GetSpec().BotName)
+	require.Equal(t, ident.BotInstanceID, botInstance.GetSpec().InstanceId)
+
+	// The initial authentication record should be sane
+	ia := botInstance.GetStatus().InitialAuthentication
+	require.NotNil(t, ia)
+	require.Equal(t, int32(1), ia.Generation)
+	require.Equal(t, string(types.JoinMethodToken), ia.JoinMethod)
+	require.Equal(t, token.GetSafeName(), ia.JoinToken)
+
+	// The latest authentications field should contain the same record (and
+	// only that record.)
+	require.Len(t, botInstance.GetStatus().LatestAuthentications, 1)
+	require.EqualExportedValues(t, ia, botInstance.GetStatus().LatestAuthentications[0])
+}
+
 // TestRegisterBotCertificateGenerationStolen simulates a stolen renewable
 // certificate where a generation check is expected to fail.
 func TestRegisterBotCertificateGenerationStolen(t *testing.T) {
diff --git a/lib/auth/join.go b/lib/auth/join.go
index e887f6fd922b5..91307b79ba34b 100644
--- a/lib/auth/join.go
+++ b/lib/auth/join.go
@@ -30,8 +30,11 @@ import (
 	"github.com/gravitational/trace"
 	"github.com/sirupsen/logrus"
 	"google.golang.org/grpc/peer"
+	"google.golang.org/protobuf/types/known/structpb"
+	"google.golang.org/protobuf/types/known/timestamppb"
 
 	"github.com/gravitational/teleport/api/client/proto"
+	machineidv1pb "github.com/gravitational/teleport/api/gen/proto/go/teleport/machineid/v1"
 	"github.com/gravitational/teleport/api/types"
 	apievents "github.com/gravitational/teleport/api/types/events"
 	"github.com/gravitational/teleport/lib/auth/machineid/machineidv1"
@@ -346,24 +349,7 @@ func (a *Server) generateCertsBot(
 		expires = *req.Expires
 	}
 
-	certs, err := a.generateInitialBotCerts(
-		ctx, botName, machineidv1.BotResourceName(botName), req.RemoteAddr, req.PublicSSHKey, expires, renewable,
-	)
-	if err != nil {
-		return nil, trace.Wrap(err)
-	}
-
-	if shouldDeleteToken {
-		// delete ephemeral bot join tokens so they can't be re-used
-		if err := a.DeleteToken(ctx, provisionToken.GetName()); err != nil {
-			log.WithError(err).Warnf("Could not delete bot provision token %q after generating certs",
-				provisionToken.GetSafeName(),
-			)
-		}
-	}
-
-	// Emit audit event for bot join.
-	log.Infof("Bot %q has joined the cluster.", botName)
+	// Construct a Join event to be sent later.
 	joinEvent := &apievents.BotJoin{
 		Metadata: apievents.Metadata{
 			Type: events.BotJoinEvent,
@@ -380,6 +366,20 @@ func (a *Server) generateCertsBot(
 			RemoteAddr: req.RemoteAddr,
 		},
 	}
+
+	auth := &machineidv1pb.BotInstanceStatusAuthentication{
+		AuthenticatedAt: timestamppb.New(a.GetClock().Now()),
+		// TODO: GetSafeName may not return an appropriate value for later
+		// comparison / locking purposes, and this also shouldn't contain
+		// secrets. Should we hash it?
+		JoinToken:  provisionToken.GetSafeName(),
+		JoinMethod: string(provisionToken.GetJoinMethod()),
+		PublicKey:  req.PublicTLSKey,
+
+		// Note: Generation will be set during `generateInitialBotCerts()` as
+		// needed.
+	}
+
 	if joinAttributeSrc != nil {
 		attributes, err := joinAttributeSrc.JoinAuditAttributes()
 		if err != nil {
@@ -389,7 +389,32 @@ func (a *Server) generateCertsBot(
 		if err != nil {
 			log.WithError(err).Warn("Unable to encode join attributes for audit event.")
 		}
+
+		auth.Metadata, err = structpb.NewStruct(attributes)
+		if err != nil {
+			log.WithError(err).Warn("Unable to encode struct value for join metadata.")
+		}
 	}
+
+	certs, err := a.generateInitialBotCerts(
+		ctx, botName, machineidv1.BotResourceName(botName), req.RemoteAddr, req.PublicSSHKey, expires, renewable, auth,
+	)
+	if err != nil {
+		return nil, trace.Wrap(err)
+	}
+
+	if shouldDeleteToken {
+		// delete ephemeral bot join tokens so they can't be re-used
+		if err := a.DeleteToken(ctx, provisionToken.GetName()); err != nil {
+			log.WithError(err).Warnf("Could not delete bot provision token %q after generating certs",
+				provisionToken.GetSafeName(),
+			)
+		}
+	}
+
+	// Emit audit event for bot join.
+	log.Infof("Bot %q has joined the cluster.", botName)
+
 	if err := a.emitter.EmitAuditEvent(ctx, joinEvent); err != nil {
 		log.WithError(err).Warn("Failed to emit bot join event.")
 	}
diff --git a/lib/auth/keygen/keygen.go b/lib/auth/keygen/keygen.go
index 8326febee7162..ce8a26dd78dfe 100644
--- a/lib/auth/keygen/keygen.go
+++ b/lib/auth/keygen/keygen.go
@@ -197,6 +197,9 @@ func (k *Keygen) GenerateUserCertWithoutValidation(c services.UserCertParams) ([
 	if c.BotName != "" {
 		cert.Permissions.Extensions[teleport.CertExtensionBotName] = c.BotName
 	}
+	if c.BotInstanceID != "" {
+		cert.Permissions.Extensions[teleport.CertExtensionBotInstanceID] = c.BotInstanceID
+	}
 	if c.AllowedResourceIDs != "" {
 		cert.Permissions.Extensions[teleport.CertExtensionAllowedResources] = c.AllowedResourceIDs
 	}
diff --git a/lib/auth/machineid/machineidv1/bot_instance_experiment/experiment.go b/lib/auth/machineid/machineidv1/bot_instance_experiment/experiment.go
new file mode 100644
index 0000000000000..a72e81f55f7ed
--- /dev/null
+++ b/lib/auth/machineid/machineidv1/bot_instance_experiment/experiment.go
@@ -0,0 +1,40 @@
+/*
+ * Teleport
+ * Copyright (C) 2024  Gravitational, Inc.
+ *
+ * This program is free software: you can redistribute it and/or modify
+ * it under the terms of the GNU Affero General Public License as published by
+ * the Free Software Foundation, either version 3 of the License, or
+ * (at your option) any later version.
+ *
+ * This program is distributed in the hope that it will be useful,
+ * but WITHOUT ANY WARRANTY; without even the implied warranty of
+ * MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+ * GNU Affero General Public License for more details.
+ *
+ * You should have received a copy of the GNU Affero General Public License
+ * along with this program.  If not, see <http://www.gnu.org/licenses/>.
+ */
+
+package experiment
+
+import (
+	"os"
+	"sync/atomic"
+)
+
+var enabled = atomic.Bool{}
+
+func init() {
+	enabled.Store(os.Getenv("BOT_INSTANCE_EXPERIMENT") == "1")
+}
+
+// Enabled returns true if the bot instance experiment is enabled.
+func Enabled() bool {
+	return enabled.Load()
+}
+
+// SetEnabled sets the bot instance experiment flag to the given value.
+func SetEnabled(value bool) {
+	enabled.Store(value)
+}
diff --git a/lib/auth/machineid/machineidv1/bot_instance_service.go b/lib/auth/machineid/machineidv1/bot_instance_service.go
index 3d07f7ebbcfa7..8947cb27242c1 100644
--- a/lib/auth/machineid/machineidv1/bot_instance_service.go
+++ b/lib/auth/machineid/machineidv1/bot_instance_service.go
@@ -21,6 +21,7 @@ package machineidv1
 import (
 	"context"
 	"log/slog"
+	"time"
 
 	"github.com/gravitational/trace"
 	"github.com/jonboulle/clockwork"
@@ -33,6 +34,18 @@ import (
 	"github.com/gravitational/teleport/lib/services"
 )
 
+const (
+	// AuthenticationHistoryLimit is the maximum number of authentication
+	// records to be recorded in a bot instance's .Status.LatestAuthentications
+	// field.
+	AuthenticationHistoryLimit = 10
+
+	// ExpiryMargin is the duration added to bot instance expiration times to
+	// ensure the instance remains accessible until shortly after the last
+	// issued certificate expires.
+	ExpiryMargin = time.Minute * 5
+)
+
 // BotInstanceServiceConfig holds configuration options for the BotInstance gRPC
 // service.
 type BotInstanceServiceConfig struct {
diff --git a/lib/services/authority.go b/lib/services/authority.go
index d00d3d00fc3df..fdcc8d40820d2 100644
--- a/lib/services/authority.go
+++ b/lib/services/authority.go
@@ -380,6 +380,9 @@ type UserCertParams struct {
 	// BotName is set to the name of the bot, if the user is a Machine ID bot user.
 	// Empty for human users.
 	BotName string
+	// BotInstanceID is the unique identifier for the bot instance, if this is a
+	// Machine ID bot. It is empty for human users.
+	BotInstanceID string
 	// AllowedResourceIDs lists the resources the user should be able to access.
 	AllowedResourceIDs string
 	// ConnectionDiagnosticID references the ConnectionDiagnostic that we should use to append traces when testing a Connection.
diff --git a/lib/services/local/bot_instance.go b/lib/services/local/bot_instance.go
index 1c2d55bbf7a0c..2db2712473daa 100644
--- a/lib/services/local/bot_instance.go
+++ b/lib/services/local/bot_instance.go
@@ -21,7 +21,6 @@ import (
 
 	"github.com/gravitational/trace"
 	"github.com/jonboulle/clockwork"
-	"google.golang.org/protobuf/types/known/timestamppb"
 
 	headerv1 "github.com/gravitational/teleport/api/gen/proto/go/teleport/header/v1"
 	machineidv1 "github.com/gravitational/teleport/api/gen/proto/go/teleport/machineid/v1"
@@ -61,26 +60,22 @@ func NewBotInstanceService(backend backend.Backend, clock clockwork.Clock) (*Bot
 
 // CreateBotInstance inserts a new BotInstance into the backend.
 //
-// Note that new BotInstances must have a nil metadata field; this will be
-// generated automatically from the spec upon insert.
+// Note that new BotInstances will have their .Metadata.Name overwritten by the
+// instance UUID.
 func (b *BotInstanceService) CreateBotInstance(ctx context.Context, instance *machineidv1.BotInstance) (*machineidv1.BotInstance, error) {
 	if err := services.ValidateBotInstance(instance); err != nil {
 		return nil, trace.Wrap(err)
 	}
 
-	if instance.Metadata != nil {
-		return nil, trace.BadParameter("metadata should be nil; initial parameters should be set in spec")
-	}
-
 	instance.Kind = types.KindBotInstance
 	instance.Version = types.V1
-	instance.Metadata = &headerv1.Metadata{Name: instance.Spec.InstanceId}
 
-	if instance.Spec.Ttl != nil {
-		expires := b.clock.Now().Add(instance.Spec.Ttl.AsDuration())
-		instance.Metadata.Expires = timestamppb.New(expires)
+	if instance.Metadata == nil {
+		instance.Metadata = &headerv1.Metadata{}
 	}
 
+	instance.Metadata.Name = instance.Spec.InstanceId
+
 	serviceWithPrefix := b.service.WithPrefix(instance.Spec.BotName)
 	created, err := serviceWithPrefix.CreateResource(ctx, instance)
 	return created, trace.Wrap(err)
@@ -142,6 +137,10 @@ func (b *BotInstanceService) PatchBotInstance(
 			return nil, trace.BadParameter("metadata.name: cannot be patched")
 		case updated.GetMetadata().GetRevision() != existing.GetMetadata().GetRevision():
 			return nil, trace.BadParameter("metadata.revision: cannot be patched")
+		case updated.GetSpec().GetInstanceId() != existing.GetSpec().GetInstanceId():
+			return nil, trace.BadParameter("spec.instance_id: cannot be patched")
+		case updated.GetSpec().GetBotName() != existing.GetSpec().GetBotName():
+			return nil, trace.BadParameter("spec.bot_name: cannot be patched")
 		}
 
 		serviceWithPrefix := b.service.WithPrefix(botName)
diff --git a/lib/services/local/bot_instance_test.go b/lib/services/local/bot_instance_test.go
index 62f6a3a2585c1..68c3eb040c62e 100644
--- a/lib/services/local/bot_instance_test.go
+++ b/lib/services/local/bot_instance_test.go
@@ -27,7 +27,7 @@ import (
 	"github.com/gravitational/trace"
 	"github.com/jonboulle/clockwork"
 	"github.com/stretchr/testify/require"
-	"google.golang.org/protobuf/types/known/durationpb"
+	"google.golang.org/protobuf/types/known/timestamppb"
 
 	headerv1 "github.com/gravitational/teleport/api/gen/proto/go/teleport/header/v1"
 	machineidv1 "github.com/gravitational/teleport/api/gen/proto/go/teleport/machineid/v1"
@@ -59,13 +59,6 @@ func newBotInstance(botName string, fns ...func(*machineidv1.BotInstance)) *mach
 	return bi
 }
 
-// withBotInstanceTTL apples a TTL to the bot instance
-func withBotInstanceTTL(d time.Duration) func(*machineidv1.BotInstance) {
-	return func(bi *machineidv1.BotInstance) {
-		bi.Spec.Ttl = durationpb.New(d)
-	}
-}
-
 // withBotInstanceInvalidMetadata modifies a BotInstance such that it should
 // raise an error during an insert attempt.
 func withBotInstanceInvalidMetadata() func(*machineidv1.BotInstance) {
@@ -76,6 +69,18 @@ func withBotInstanceInvalidMetadata() func(*machineidv1.BotInstance) {
 	}
 }
 
+// withBotInstanceExpiry sets the .Metadata.Expires field of a bot instance to
+// the given timestamp.
+func withBotInstanceExpiry(expiry time.Time) func(*machineidv1.BotInstance) {
+	return func(bi *machineidv1.BotInstance) {
+		if bi.Metadata == nil {
+			bi.Metadata = &headerv1.Metadata{}
+		}
+
+		bi.Metadata.Expires = timestamppb.New(expiry)
+	}
+}
+
 // createInstances creates new bot instances for the named bot with random UUIDs
 func createInstances(t *testing.T, ctx context.Context, service *BotInstanceService, botName string, count int) map[string]struct{} {
 	t.Helper()
@@ -132,11 +137,18 @@ func TestBotInstanceCreateMetadata(t *testing.T) {
 		{
 			name:        "non-nil metadata",
 			instance:    newBotInstance("foo", withBotInstanceInvalidMetadata()),
-			assertError: require.Error,
-			assertValue: require.Nil,
+			assertError: require.NoError,
+			assertValue: func(t require.TestingT, i interface{}, _ ...interface{}) {
+				bi, ok := i.(*machineidv1.BotInstance)
+				require.True(t, ok)
+
+				// .Metadata.Name should be overwritten with the correct value
+				require.Equal(t, bi.Spec.InstanceId, bi.Metadata.Name)
+				require.Nil(t, bi.Metadata.Expires)
+			},
 		},
 		{
-			name:        "valid without ttl",
+			name:        "valid without expiry",
 			instance:    newBotInstance("foo"),
 			assertError: require.NoError,
 			assertValue: func(t require.TestingT, i interface{}, _ ...interface{}) {
@@ -148,8 +160,8 @@ func TestBotInstanceCreateMetadata(t *testing.T) {
 			},
 		},
 		{
-			name:        "valid with ttl",
-			instance:    newBotInstance("foo", withBotInstanceTTL(time.Hour)),
+			name:        "valid with expiry",
+			instance:    newBotInstance("foo", withBotInstanceExpiry(clock.Now().Add(time.Hour))),
 			assertError: require.NoError,
 			assertValue: func(t require.TestingT, i interface{}, _ ...interface{}) {
 				bi, ok := i.(*machineidv1.BotInstance)
diff --git a/lib/srv/authhandlers.go b/lib/srv/authhandlers.go
index 8404b02fc0ce9..d80f5704acfe4 100644
--- a/lib/srv/authhandlers.go
+++ b/lib/srv/authhandlers.go
@@ -209,6 +209,9 @@ func (h *AuthHandlers) CreateIdentityContext(sconn *ssh.ServerConn) (IdentityCon
 	if botName, ok := certificate.Extensions[teleport.CertExtensionBotName]; ok {
 		identity.BotName = botName
 	}
+	if botInstanceID, ok := certificate.Extensions[teleport.CertExtensionBotInstanceID]; ok {
+		identity.BotInstanceID = botInstanceID
+	}
 	if generationStr, ok := certificate.Extensions[teleport.CertExtensionGeneration]; ok {
 		generation, err := strconv.ParseUint(generationStr, 10, 64)
 		if err != nil {
diff --git a/lib/srv/ctx.go b/lib/srv/ctx.go
index cccf7e0f95ae6..f6f682eb61e8b 100644
--- a/lib/srv/ctx.go
+++ b/lib/srv/ctx.go
@@ -280,6 +280,10 @@ type IdentityContext struct {
 	// with, if any.
 	BotName string
 
+	// BotInstanceID is the unique identifier of the Machine ID bot instance
+	// this identity is associated with, if any.
+	BotInstanceID string
+
 	// AllowedResourceIDs lists the resources this identity should be allowed to
 	// access
 	AllowedResourceIDs []types.ResourceID
diff --git a/lib/tlsca/ca.go b/lib/tlsca/ca.go
index ff67923ae8ae6..151c0ef4aff72 100644
--- a/lib/tlsca/ca.go
+++ b/lib/tlsca/ca.go
@@ -184,6 +184,9 @@ type Identity struct {
 	// BotName indicates the name of the Machine ID bot this identity was issued
 	// to, if any.
 	BotName string
+	// BotInstanceID is a unique identifier for Machine ID bots that is
+	// persisted through renewals.
+	BotInstanceID string
 	// AllowedResourceIDs lists the resources the identity should be allowed to
 	// access.
 	AllowedResourceIDs []types.ResourceID
@@ -528,6 +531,10 @@ var (
 	// RequestedDatabaseRolesExtensionOID is an extension OID used when
 	// encoding/decoding requested database roles.
 	RequestedDatabaseRolesExtensionOID = asn1.ObjectIdentifier{1, 3, 9999, 2, 19}
+
+	// BotInstanceASN1ExtensionOID is an extension that encodes a unique bot
+	// instance identifier into a certificate.
+	BotInstanceASN1ExtensionOID = asn1.ObjectIdentifier{1, 3, 9999, 2, 20}
 )
 
 // Device Trust OIDs.
@@ -810,6 +817,14 @@ func (id *Identity) Subject() (pkix.Name, error) {
 			})
 	}
 
+	if id.BotInstanceID != "" {
+		subject.ExtraNames = append(subject.ExtraNames,
+			pkix.AttributeTypeAndValue{
+				Type:  BotInstanceASN1ExtensionOID,
+				Value: id.BotInstanceID,
+			})
+	}
+
 	if len(id.AllowedResourceIDs) > 0 {
 		allowedResourcesStr, err := types.ResourceIDsToString(id.AllowedResourceIDs)
 		if err != nil {
@@ -1050,6 +1065,11 @@ func FromSubject(subject pkix.Name, expires time.Time) (*Identity, error) {
 			if ok {
 				id.BotName = val
 			}
+		case attr.Type.Equal(BotInstanceASN1ExtensionOID):
+			val, ok := attr.Value.(string)
+			if ok {
+				id.BotInstanceID = val
+			}
 		case attr.Type.Equal(AllowedResourcesASN1ExtensionOID):
 			allowedResourcesStr, ok := attr.Value.(string)
 			if ok {