diff --git a/connection/quic_datagram_v3.go b/connection/quic_datagram_v3.go
new file mode 100644
index 00000000..3921d66c
--- /dev/null
+++ b/connection/quic_datagram_v3.go
@@ -0,0 +1,48 @@
+package connection
+
+import (
+	"context"
+	"fmt"
+	"net"
+	"time"
+
+	"github.com/google/uuid"
+	"github.com/quic-go/quic-go"
+	"github.com/rs/zerolog"
+
+	cfdquic "github.com/cloudflare/cloudflared/quic/v3"
+	"github.com/cloudflare/cloudflared/tunnelrpc/pogs"
+)
+
+type datagramV3Connection struct {
+	conn quic.Connection
+	// datagramMuxer mux/demux datagrams from quic connection
+	datagramMuxer cfdquic.DatagramConn
+	logger        *zerolog.Logger
+}
+
+func NewDatagramV3Connection(ctx context.Context,
+	conn quic.Connection,
+	sessionManager cfdquic.SessionManager,
+	logger *zerolog.Logger,
+) DatagramSessionHandler {
+	datagramMuxer := cfdquic.NewDatagramConn(conn, sessionManager, logger)
+
+	return &datagramV3Connection{
+		conn,
+		datagramMuxer,
+		logger,
+	}
+}
+
+func (d *datagramV3Connection) Serve(ctx context.Context) error {
+	return d.datagramMuxer.Serve(ctx)
+}
+
+func (d *datagramV3Connection) RegisterUdpSession(ctx context.Context, sessionID uuid.UUID, dstIP net.IP, dstPort uint16, closeAfterIdleHint time.Duration, traceContext string) (*pogs.RegisterUdpSessionResponse, error) {
+	return nil, fmt.Errorf("datagram v3 does not support RegisterUdpSession RPC")
+}
+
+func (d *datagramV3Connection) UnregisterUdpSession(ctx context.Context, sessionID uuid.UUID, message string) error {
+	return fmt.Errorf("datagram v3 does not support UnregisterUdpSession RPC")
+}
diff --git a/supervisor/supervisor.go b/supervisor/supervisor.go
index 8dde4e76..8d68f6b7 100644
--- a/supervisor/supervisor.go
+++ b/supervisor/supervisor.go
@@ -12,7 +12,9 @@ import (
 
 	"github.com/cloudflare/cloudflared/connection"
 	"github.com/cloudflare/cloudflared/edgediscovery"
+	"github.com/cloudflare/cloudflared/ingress"
 	"github.com/cloudflare/cloudflared/orchestration"
+	v3 "github.com/cloudflare/cloudflared/quic/v3"
 	"github.com/cloudflare/cloudflared/retry"
 	"github.com/cloudflare/cloudflared/signal"
 	"github.com/cloudflare/cloudflared/tunnelstate"
@@ -80,9 +82,12 @@ func NewSupervisor(config *TunnelConfig, orchestrator *orchestration.Orchestrato
 	edgeAddrHandler := NewIPAddrFallback(config.MaxEdgeAddrRetries)
 	edgeBindAddr := config.EdgeBindAddr
 
+	sessionManager := v3.NewSessionManager(config.Log, ingress.DialUDPAddrPort)
+
 	edgeTunnelServer := EdgeTunnelServer{
 		config:            config,
 		orchestrator:      orchestrator,
+		sessionManager:    sessionManager,
 		edgeAddrs:         edgeIPs,
 		edgeAddrHandler:   edgeAddrHandler,
 		edgeBindAddr:      edgeBindAddr,
diff --git a/supervisor/tunnel.go b/supervisor/tunnel.go
index 7de2cbd0..3e6ca86a 100644
--- a/supervisor/tunnel.go
+++ b/supervisor/tunnel.go
@@ -7,6 +7,7 @@ import (
 	"net"
 	"net/netip"
 	"runtime/debug"
+	"slices"
 	"strings"
 	"sync"
 	"time"
@@ -24,6 +25,7 @@ import (
 	"github.com/cloudflare/cloudflared/management"
 	"github.com/cloudflare/cloudflared/orchestration"
 	quicpogs "github.com/cloudflare/cloudflared/quic"
+	v3 "github.com/cloudflare/cloudflared/quic/v3"
 	"github.com/cloudflare/cloudflared/retry"
 	"github.com/cloudflare/cloudflared/signal"
 	"github.com/cloudflare/cloudflared/tunnelrpc/pogs"
@@ -87,14 +89,6 @@ func (c *TunnelConfig) connectionOptions(originLocalAddr string, numPreviousAtte
 	}
 }
 
-func (c *TunnelConfig) SupportedFeatures() []string {
-	supported := []string{features.FeatureSerializedHeaders}
-	if c.NamedTunnel == nil {
-		supported = append(supported, features.FeatureQuickReconnects)
-	}
-	return supported
-}
-
 func StartTunnelDaemon(
 	ctx context.Context,
 	config *TunnelConfig,
@@ -181,6 +175,7 @@ func (f *ipAddrFallback) ShouldGetNewAddress(connIndex uint8, err error) (needsN
 type EdgeTunnelServer struct {
 	config            *TunnelConfig
 	orchestrator      *orchestration.Orchestrator
+	sessionManager    v3.SessionManager
 	edgeAddrHandler   EdgeAddrHandler
 	edgeAddrs         *edgediscovery.Edge
 	edgeBindAddr      net.IP
@@ -605,14 +600,24 @@ func (e *EdgeTunnelServer) serveQUIC(
 		return err, true
 	}
 
-	datagramSessionManager := connection.NewDatagramV2Connection(
-		ctx,
-		conn,
-		e.config.PacketConfig,
-		e.config.RPCTimeout,
-		e.config.WriteStreamTimeout,
-		connLogger.Logger(),
-	)
+	var datagramSessionManager connection.DatagramSessionHandler
+	if slices.Contains(connOptions.Client.Features, features.FeatureDatagramV3) {
+		datagramSessionManager = connection.NewDatagramV3Connection(
+			ctx,
+			conn,
+			e.sessionManager,
+			connLogger.Logger(),
+		)
+	} else {
+		datagramSessionManager = connection.NewDatagramV2Connection(
+			ctx,
+			conn,
+			e.config.PacketConfig,
+			e.config.RPCTimeout,
+			e.config.WriteStreamTimeout,
+			connLogger.Logger(),
+		)
+	}
 
 	// Wrap the [quic.Connection] as a TunnelConnection
 	tunnelConn, err := connection.NewTunnelConnection(