diff --git a/contrib/check-config.sh b/contrib/check-config.sh
index af7d8a7de5..3e910ae956 100755
--- a/contrib/check-config.sh
+++ b/contrib/check-config.sh
@@ -128,6 +128,16 @@ check_device() {
 	fi
 }
 
+check_sysctl() {
+	val=$(sysctl -n $1)
+	want=$2
+	if [ "$val" = "$want" ]; then
+		wrap_good "sysctl $1" "enabled"
+	else
+		wrap_bad "sysctl $1" "disabled"
+	fi
+}
+
 if [ ! -e "$CONFIG" ]; then
 	wrap_warning "warning: $CONFIG does not exist, searching other paths for kernel config ..."
 	for tryConfig in $possibleConfigs; do
@@ -343,6 +353,10 @@ if ! is_set EXT4_FS || ! is_set EXT4_FS_POSIX_ACL || ! is_set EXT4_FS_SECURITY;
 fi
 
 echo '- Network Drivers:'
+echo "  - \"$(wrap_color 'bridge' blue)\":"
+check_sysctl net.ipv4.ip_forward 1 | sed 's/^/    - /'
+check_sysctl net.ipv6.conf.all.forwarding 1 | sed 's/^/    - /'
+check_sysctl net.ipv6.conf.default.forwarding 1 | sed 's/^/    - /'
 echo "  - \"$(wrap_color 'overlay' blue)\":"
 check_flags VXLAN BRIDGE_VLAN_FILTERING | sed 's/^/    /'
 echo '      Optional (for encrypted networks):'
diff --git a/contrib/dockerd-rootless.sh b/contrib/dockerd-rootless.sh
index f798cd09dd..3ded28f6dd 100755
--- a/contrib/dockerd-rootless.sh
+++ b/contrib/dockerd-rootless.sh
@@ -199,5 +199,12 @@ else
 		mount_directory /etc/ssl "--rbind"
 	fi
 
+	# When running with --firewall-backend=nftables, IP forwarding needs to be enabled
+	# because the daemon won't enable it. IP forwarding is harmless in the rootless
+	# netns, there's only a single external interface and only Docker uses the netns.
+	# So, always enable IPv4 and IPv6 forwarding.
+	sysctl -w net.ipv4.ip_forward=1
+	sysctl -w net.ipv6.conf.all.forwarding=1
+
 	exec "$dockerd" "$@"
 fi
diff --git a/daemon/libnetwork/drivers/bridge/bridge_linux.go b/daemon/libnetwork/drivers/bridge/bridge_linux.go
index 84e66a7715..8af622e318 100644
--- a/daemon/libnetwork/drivers/bridge/bridge_linux.go
+++ b/daemon/libnetwork/drivers/bridge/bridge_linux.go
@@ -556,7 +556,7 @@ var newFirewaller = func(ctx context.Context, config firewaller.Config) (firewal
 		// cleaner can't clean up network or port-specific rules that may have been added
 		// to iptables built-in chains. So, if cleanup is needed, give the cleaner to
 		// the nftabler. Then, it'll use it to delete old rules as networks are restored.
-		fw.(firewaller.FirewallCleanerSetter).SetFirewallCleaner(iptabler.NewCleaner(ctx, config))
+		fw.SetFirewallCleaner(iptabler.NewCleaner(ctx, config))
 		return fw, nil
 	}
 
@@ -880,14 +880,28 @@ func (d *driver) createNetwork(ctx context.Context, config *networkConfiguration
 			config.EnableIPv4 && d.config.EnableIPForwarding,
 			"setupIPv4Forwarding",
 			func(*networkConfiguration, *bridgeInterface) error {
-				return setupIPv4Forwarding(d.firewaller, d.config.EnableIPTables && !d.config.DisableFilterForwardDrop)
+				ffd, ok := d.firewaller.(filterForwardDropper)
+				if !ok {
+					// The firewaller can't drop non-Docker forwarding. It's up to the user to enable
+					// forwarding on their host, and configure their firewall appropriately.
+					return checkIPv4Forwarding()
+				}
+				// Enable forwarding and set a default-drop forwarding policy if necessary.
+				return setupIPv4Forwarding(ffd, d.config.EnableIPTables && !d.config.DisableFilterForwardDrop)
 			},
 		},
 		{
 			config.EnableIPv6 && d.config.EnableIPForwarding,
 			"setupIPv6Forwarding",
 			func(*networkConfiguration, *bridgeInterface) error {
-				return setupIPv6Forwarding(d.firewaller, d.config.EnableIP6Tables && !d.config.DisableFilterForwardDrop)
+				ffd, ok := d.firewaller.(filterForwardDropper)
+				if !ok {
+					// The firewaller can't drop non-Docker forwarding. It's up to the user to enable
+					// forwarding on their host, and configure their firewall appropriately.
+					return checkIPv6Forwarding()
+				}
+				// Enable forwarding and set a default-drop forwarding policy if necessary.
+				return setupIPv6Forwarding(ffd, d.config.EnableIP6Tables && !d.config.DisableFilterForwardDrop)
 			},
 		},
 
diff --git a/daemon/libnetwork/drivers/bridge/bridge_store.go b/daemon/libnetwork/drivers/bridge/bridge_store.go
index 92a7dc20d1..78dce7e53d 100644
--- a/daemon/libnetwork/drivers/bridge/bridge_store.go
+++ b/daemon/libnetwork/drivers/bridge/bridge_store.go
@@ -13,7 +13,7 @@ import (
 	"github.com/containerd/log"
 	"github.com/moby/moby/v2/daemon/internal/otelutil"
 	"github.com/moby/moby/v2/daemon/libnetwork/datastore"
-	"github.com/moby/moby/v2/daemon/libnetwork/drivers/bridge/internal/firewaller"
+	"github.com/moby/moby/v2/daemon/libnetwork/drivers/bridge/internal/nftabler"
 	"github.com/moby/moby/v2/daemon/libnetwork/portmapperapi"
 	"github.com/moby/moby/v2/daemon/libnetwork/types"
 	"go.opentelemetry.io/otel"
@@ -43,8 +43,8 @@ func (d *driver) initStore() error {
 
 	// If there's a firewall cleaner, it's done its job by cleaning up rules
 	// belonging to the restored networks. So, drop it.
-	if fcs, ok := d.firewaller.(firewaller.FirewallCleanerSetter); ok {
-		fcs.SetFirewallCleaner(nil)
+	if nft, ok := d.firewaller.(*nftabler.Nftabler); ok {
+		nft.SetFirewallCleaner(nil)
 	}
 
 	return nil
diff --git a/daemon/libnetwork/drivers/bridge/internal/firewaller/firewaller.go b/daemon/libnetwork/drivers/bridge/internal/firewaller/firewaller.go
index 743b03c23e..9ab68aaa58 100644
--- a/daemon/libnetwork/drivers/bridge/internal/firewaller/firewaller.go
+++ b/daemon/libnetwork/drivers/bridge/internal/firewaller/firewaller.go
@@ -76,9 +76,6 @@ type Firewaller interface {
 	// NewNetwork returns an object that can be used to add published ports and legacy
 	// links for a bridge network.
 	NewNetwork(ctx context.Context, nc NetworkConfig) (Network, error)
-	// FilterForwardDrop sets the default policy of the FORWARD chain in the filter
-	// table to DROP.
-	FilterForwardDrop(ctx context.Context, ipv IPVersion) error
 }
 
 // Network can be used to manipulate firewall rules for a bridge network.
@@ -110,12 +107,6 @@ type Network interface {
 	DelLink(ctx context.Context, parentIP, childIP netip.Addr, ports []types.TransportPort)
 }
 
-// FirewallCleanerSetter is an optional interface for a Firewaller.
-type FirewallCleanerSetter interface {
-	// SetFirewallCleaner replaces the FirewallCleaner (possibly with 'nil').
-	SetFirewallCleaner(FirewallCleaner)
-}
-
 // FirewallCleaner is used to delete rules created by previous incarnations of
 // the daemon. On startup, once a Firewaller implementation has been selected, if
 // rules may have been left behind by a different Firewaller implementation, get
diff --git a/daemon/libnetwork/drivers/bridge/internal/firewaller/stub.go b/daemon/libnetwork/drivers/bridge/internal/firewaller/stub.go
index cf884edd26..f09df48415 100644
--- a/daemon/libnetwork/drivers/bridge/internal/firewaller/stub.go
+++ b/daemon/libnetwork/drivers/bridge/internal/firewaller/stub.go
@@ -15,7 +15,6 @@ import (
 type StubFirewaller struct {
 	Config
 	Networks map[string]*StubFirewallerNetwork
-	FFD      map[IPVersion]bool // filter forward drop
 }
 
 func NewStubFirewaller(config Config) *StubFirewaller {
@@ -24,7 +23,6 @@ func NewStubFirewaller(config Config) *StubFirewaller {
 		// A real Firewaller shouldn't hold on to its own networks, the bridge driver is doing that.
 		// But, for unit tests cross-checking the driver, this is useful.
 		Networks: make(map[string]*StubFirewallerNetwork),
-		FFD:      make(map[IPVersion]bool),
 	}
 }
 
@@ -41,11 +39,6 @@ func (fw *StubFirewaller) NewNetwork(_ context.Context, nc NetworkConfig) (Netwo
 	return nw, nil
 }
 
-func (fw *StubFirewaller) FilterForwardDrop(_ context.Context, ipv IPVersion) error {
-	fw.FFD[ipv] = true
-	return nil
-}
-
 type stubFirewallerLink struct {
 	parentIP netip.Addr
 	childIP  netip.Addr
diff --git a/daemon/libnetwork/drivers/bridge/internal/iptabler/cleaner.go b/daemon/libnetwork/drivers/bridge/internal/iptabler/cleaner.go
index 98f3f5f340..1de527b08b 100644
--- a/daemon/libnetwork/drivers/bridge/internal/iptabler/cleaner.go
+++ b/daemon/libnetwork/drivers/bridge/internal/iptabler/cleaner.go
@@ -17,7 +17,7 @@ type iptablesCleaner struct {
 }
 
 // NewCleaner checks for iptables rules left behind by an old daemon that was using
-// the iptabler.
+// the Iptabler.
 //
 // If there are old rules present, it deletes as much as possible straight away
 // (user-defined chains and jumps from the built-in chains).
@@ -46,6 +46,13 @@ func NewCleaner(ctx context.Context, config firewaller.Config) firewaller.Firewa
 		_ = t.DeleteJumpRule(iptables.Filter, "FORWARD", DockerForwardChain)
 		_ = deleteLegacyTopLevelRules(ctx, t, ipv)
 		removeIPChains(ctx, ipv)
+		// The iptables chains will no longer have Docker's ACCEPT rules. So, if the
+		// filter-FORWARD chain has policy DROP (possibly set by Docker when it enabled
+		// IP forwarding), packets accepted by nftables chains will still be processed by
+		// iptables and dropped. It's the user's responsibility to sort that out.
+		if t.HasPolicy("filter", "FORWARD", iptables.Drop) {
+			log.G(ctx).WithField("ipv", ipv).Warn("Network traffic for published ports may be dropped, iptables chain FORWARD has policy DROP.")
+		}
 		return true
 	}
 	cleaned4 := clean(iptables.IPv4, config.IPv4)
@@ -62,7 +69,7 @@ func (ic iptablesCleaner) DelNetwork(ctx context.Context, nc firewaller.NetworkC
 	}
 	n := network{
 		config: nc,
-		ipt:    &iptabler{config: ic.config},
+		ipt:    &Iptabler{config: ic.config},
 	}
 	if ic.config.IPv4 && nc.Config4.Prefix.IsValid() {
 		_ = deleteLegacyFilterRules(iptables.IPv4, nc.IfName)
@@ -77,7 +84,7 @@ func (ic iptablesCleaner) DelNetwork(ctx context.Context, nc firewaller.NetworkC
 func (ic iptablesCleaner) DelEndpoint(ctx context.Context, nc firewaller.NetworkConfig, epIPv4, epIPv6 netip.Addr) {
 	n := network{
 		config: nc,
-		ipt:    &iptabler{config: ic.config},
+		ipt:    &Iptabler{config: ic.config},
 	}
 	if n.ipt.config.IPv4 && epIPv4.IsValid() {
 		_ = n.filterDirectAccess(ctx, iptables.IPv4, n.config.Config4, epIPv4, false)
@@ -90,7 +97,7 @@ func (ic iptablesCleaner) DelEndpoint(ctx context.Context, nc firewaller.Network
 func (ic iptablesCleaner) DelPorts(ctx context.Context, nc firewaller.NetworkConfig, pbs []types.PortBinding) {
 	n := network{
 		config: nc,
-		ipt:    &iptabler{config: ic.config},
+		ipt:    &Iptabler{config: ic.config},
 	}
 	_ = n.DelPorts(ctx, pbs)
 }
diff --git a/daemon/libnetwork/drivers/bridge/internal/iptabler/iptabler.go b/daemon/libnetwork/drivers/bridge/internal/iptabler/iptabler.go
index 74df0ba8b8..0a51582e3b 100644
--- a/daemon/libnetwork/drivers/bridge/internal/iptabler/iptabler.go
+++ b/daemon/libnetwork/drivers/bridge/internal/iptabler/iptabler.go
@@ -35,12 +35,12 @@ const (
 	isolationChain2 = "DOCKER-ISOLATION-STAGE-2"
 )
 
-type iptabler struct {
+type Iptabler struct {
 	config firewaller.Config
 }
 
-func NewIptabler(ctx context.Context, config firewaller.Config) (firewaller.Firewaller, error) {
-	ipt := &iptabler{config: config}
+func NewIptabler(ctx context.Context, config firewaller.Config) (*Iptabler, error) {
+	ipt := &Iptabler{config: config}
 
 	if ipt.config.IPv4 {
 		removeIPChains(ctx, iptables.IPv4)
@@ -91,7 +91,8 @@ func NewIptabler(ctx context.Context, config firewaller.Config) (firewaller.Fire
 	return ipt, nil
 }
 
-func (ipt *iptabler) FilterForwardDrop(ctx context.Context, ipv firewaller.IPVersion) error {
+// FilterForwardDrop sets the default policy of the FORWARD chain in the filter table to DROP.
+func (ipt *Iptabler) FilterForwardDrop(ctx context.Context, ipv firewaller.IPVersion) error {
 	var iptv iptables.IPVersion
 	switch ipv {
 	case firewaller.IPv4:
diff --git a/daemon/libnetwork/drivers/bridge/internal/iptabler/network.go b/daemon/libnetwork/drivers/bridge/internal/iptabler/network.go
index f80802fb35..5eef4d6690 100644
--- a/daemon/libnetwork/drivers/bridge/internal/iptabler/network.go
+++ b/daemon/libnetwork/drivers/bridge/internal/iptabler/network.go
@@ -22,11 +22,11 @@ type (
 
 type network struct {
 	config     firewaller.NetworkConfig
-	ipt        *iptabler
+	ipt        *Iptabler
 	cleanFuncs iptablesCleanFuncs
 }
 
-func (ipt *iptabler) NewNetwork(ctx context.Context, nc firewaller.NetworkConfig) (_ firewaller.Network, retErr error) {
+func (ipt *Iptabler) NewNetwork(ctx context.Context, nc firewaller.NetworkConfig) (_ firewaller.Network, retErr error) {
 	n := &network{
 		ipt:    ipt,
 		config: nc,
diff --git a/daemon/libnetwork/drivers/bridge/internal/nftabler/cleaner.go b/daemon/libnetwork/drivers/bridge/internal/nftabler/cleaner.go
index 7efbfe7a91..c57c36d654 100644
--- a/daemon/libnetwork/drivers/bridge/internal/nftabler/cleaner.go
+++ b/daemon/libnetwork/drivers/bridge/internal/nftabler/cleaner.go
@@ -11,7 +11,7 @@ import (
 	"github.com/moby/moby/v2/daemon/libnetwork/internal/nftables"
 )
 
-// Cleanup deletes all rules created by nftabler; it's intended to be used
+// Cleanup deletes all rules created by Nftabler; it's intended to be used
 // during startup, to clean up rules created by an old incarnation of the daemon
 // after switching to a different Firewaller implementation.
 func Cleanup(ctx context.Context, config firewaller.Config) {
@@ -31,6 +31,6 @@ func Cleanup(ctx context.Context, config firewaller.Config) {
 	}
 }
 
-func (nft *nftabler) SetFirewallCleaner(fc firewaller.FirewallCleaner) {
+func (nft *Nftabler) SetFirewallCleaner(fc firewaller.FirewallCleaner) {
 	nft.cleaner = fc
 }
diff --git a/daemon/libnetwork/drivers/bridge/internal/nftabler/network.go b/daemon/libnetwork/drivers/bridge/internal/nftabler/network.go
index 996cc86128..b5dd54bf27 100644
--- a/daemon/libnetwork/drivers/bridge/internal/nftabler/network.go
+++ b/daemon/libnetwork/drivers/bridge/internal/nftabler/network.go
@@ -18,10 +18,10 @@ import (
 type network struct {
 	config  firewaller.NetworkConfig
 	cleaner func(ctx context.Context) error
-	fw      *nftabler
+	fw      *Nftabler
 }
 
-func (nft *nftabler) NewNetwork(ctx context.Context, nc firewaller.NetworkConfig) (_ firewaller.Network, retErr error) {
+func (nft *Nftabler) NewNetwork(ctx context.Context, nc firewaller.NetworkConfig) (_ firewaller.Network, retErr error) {
 	n := &network{
 		fw:     nft,
 		config: nc,
diff --git a/daemon/libnetwork/drivers/bridge/internal/nftabler/nftabler.go b/daemon/libnetwork/drivers/bridge/internal/nftabler/nftabler.go
index 9d6f15c3e6..e0fe055bd9 100644
--- a/daemon/libnetwork/drivers/bridge/internal/nftabler/nftabler.go
+++ b/daemon/libnetwork/drivers/bridge/internal/nftabler/nftabler.go
@@ -45,15 +45,15 @@ const (
 	rawPreroutingPortsRuleGroup = iota + initialRuleGroup + 1
 )
 
-type nftabler struct {
+type Nftabler struct {
 	config  firewaller.Config
 	cleaner firewaller.FirewallCleaner
 	table4  nftables.TableRef
 	table6  nftables.TableRef
 }
 
-func NewNftabler(ctx context.Context, config firewaller.Config) (firewaller.Firewaller, error) {
-	nft := &nftabler{config: config}
+func NewNftabler(ctx context.Context, config firewaller.Config) (*Nftabler, error) {
+	nft := &Nftabler{config: config}
 
 	if nft.config.IPv4 {
 		var err error
@@ -85,23 +85,8 @@ func NewNftabler(ctx context.Context, config firewaller.Config) (firewaller.Fire
 	return nft, nil
 }
 
-func (nft *nftabler) getTable(ipv firewaller.IPVersion) nftables.TableRef {
-	if ipv == firewaller.IPv4 {
-		return nft.table4
-	}
-	return nft.table6
-}
-
-func (nft *nftabler) FilterForwardDrop(ctx context.Context, ipv firewaller.IPVersion) error {
-	table := nft.getTable(ipv)
-	if err := table.Chain(ctx, forwardChain).SetPolicy("drop"); err != nil {
-		return err
-	}
-	return nftApply(ctx, table)
-}
-
 // init creates the bridge driver's nftables table for IPv4 or IPv6.
-func (nft *nftabler) init(ctx context.Context, family nftables.Family) (nftables.TableRef, error) {
+func (nft *Nftabler) init(ctx context.Context, family nftables.Family) (nftables.TableRef, error) {
 	// Instantiate the table.
 	table, err := nftables.NewTable(family, dockerTable)
 	if err != nil {
diff --git a/daemon/libnetwork/drivers/bridge/setup_ip_forwarding.go b/daemon/libnetwork/drivers/bridge/setup_ip_forwarding.go
index 4f2845d0f5..0ebd4eb17d 100644
--- a/daemon/libnetwork/drivers/bridge/setup_ip_forwarding.go
+++ b/daemon/libnetwork/drivers/bridge/setup_ip_forwarding.go
@@ -4,6 +4,7 @@ package bridge
 
 import (
 	"context"
+	"errors"
 	"fmt"
 	"os"
 
@@ -17,7 +18,24 @@ const (
 	ipv6ForwardConfAll     = "/proc/sys/net/ipv6/conf/all/forwarding"
 )
 
-func setupIPv4Forwarding(fw firewaller.Firewaller, wantFilterForwardDrop bool) (retErr error) {
+type filterForwardDropper interface {
+	FilterForwardDrop(context.Context, firewaller.IPVersion) error
+}
+
+func checkIPv4Forwarding() error {
+	enabled, err := getKernelBoolParam(ipv4ForwardConf)
+	if err != nil {
+		return fmt.Errorf("checking IPv4 forwarding: %w", err)
+	}
+	if enabled {
+		return nil
+	}
+	// It's the user's responsibility to enable forwarding and secure their host. Or,
+	// start docker with --ip-forward=false to disable this check.
+	return errors.New("IPv4 forwarding is disabled: check your host's firewalling and set sysctl net.ipv4.ip_forward=1, or disable this check using daemon option --ip-forward=false")
+}
+
+func setupIPv4Forwarding(ffd filterForwardDropper, wantFilterForwardDrop bool) (retErr error) {
 	changed, err := configureIPForwarding(ipv4ForwardConf, '1')
 	if err != nil {
 		return err
@@ -34,16 +52,35 @@ func setupIPv4Forwarding(fw firewaller.Firewaller, wantFilterForwardDrop bool) (
 
 	// When enabling ip_forward set the default policy on forward chain to drop.
 	if changed && wantFilterForwardDrop {
-		if err := fw.FilterForwardDrop(context.TODO(), firewaller.IPv4); err != nil {
+		if err := ffd.FilterForwardDrop(context.TODO(), firewaller.IPv4); err != nil {
 			return err
 		}
 	}
 	return nil
 }
 
-func setupIPv6Forwarding(fw firewaller.Firewaller, wantFilterForwardDrop bool) (retErr error) {
+func checkIPv6Forwarding() error {
+	enabledDef, err := getKernelBoolParam(ipv6ForwardConfDefault)
+	if err != nil {
+		return fmt.Errorf("checking IPv6 default forwarding: %w", err)
+	}
+	enabledAll, err := getKernelBoolParam(ipv6ForwardConfAll)
+	if err != nil {
+		return fmt.Errorf("checking IPv6 global forwarding: %w", err)
+	}
+	if enabledDef && enabledAll {
+		return nil
+	}
+
+	// It's the user's responsibility to enable forwarding and secure their host. Or,
+	// start docker with --ip-forward=false to disable this check.
+	return errors.New("IPv6 global forwarding is disabled: check your host's firewalling and set sysctls net.ipv6.conf.all.forwarding=1 and net.ipv6.conf.default.forwarding=1, or disable this check using daemon option --ip-forward=false")
+}
+
+func setupIPv6Forwarding(ffd filterForwardDropper, wantFilterForwardDrop bool) (retErr error) {
 	// Set IPv6 default.forwarding, if needed.
-	// FIXME(robmry) - is it necessary to set this, setting "all" (below) does the job?
+	// Setting "all" (below) sets "default" as well, but need to check that "default" is
+	// set even if "all" is already set.
 	changedDef, err := configureIPForwarding(ipv6ForwardConfDefault, '1')
 	if err != nil {
 		return err
@@ -74,7 +111,7 @@ func setupIPv6Forwarding(fw firewaller.Firewaller, wantFilterForwardDrop bool) (
 	}
 
 	if (changedAll || changedDef) && wantFilterForwardDrop {
-		if err := fw.FilterForwardDrop(context.TODO(), firewaller.IPv6); err != nil {
+		if err := ffd.FilterForwardDrop(context.TODO(), firewaller.IPv6); err != nil {
 			return err
 		}
 	}
diff --git a/daemon/libnetwork/drivers/bridge/setup_ip_forwarding_test.go b/daemon/libnetwork/drivers/bridge/setup_ip_forwarding_test.go
index 65da1b9f79..7567c169de 100644
--- a/daemon/libnetwork/drivers/bridge/setup_ip_forwarding_test.go
+++ b/daemon/libnetwork/drivers/bridge/setup_ip_forwarding_test.go
@@ -14,19 +14,20 @@ import (
 	is "gotest.tools/v3/assert/cmp"
 )
 
-type ffdTestFirewaller struct {
-	ffd firewaller.IPVersion
-}
-
-// NewNetwork is part of interface [firewaller.Firewaller].
-func (f *ffdTestFirewaller) NewNetwork(_ context.Context, _ firewaller.NetworkConfig) (firewaller.Network, error) {
-	return nil, nil
+type ffDropper struct {
+	ffDrop4 bool
+	ffDrop6 bool
 }
 
 // FilterForwardDrop is part of interface [firewaller.Firewaller]. Just enough to check
 // it was called with the expected IPVersion.
-func (f *ffdTestFirewaller) FilterForwardDrop(_ context.Context, ipv firewaller.IPVersion) error {
-	f.ffd = ipv
+func (f *ffDropper) FilterForwardDrop(_ context.Context, ipv firewaller.IPVersion) error {
+	switch ipv {
+	case firewaller.IPv4:
+		f.ffDrop4 = true
+	case firewaller.IPv6:
+		f.ffDrop6 = true
+	}
 	return nil
 }
 
@@ -36,21 +37,16 @@ func TestSetupIPForwarding(t *testing.T) {
 	for _, wantFFD := range []bool{true, false} {
 		t.Run(fmt.Sprintf("wantFFD=%v", wantFFD), func(t *testing.T) {
 			// Disable IP Forwarding if enabled
-			_, err := configureIPForwarding(ipv4ForwardConf, '0')
-			assert.NilError(t, err)
+			setForwarding(t, '0')
 
 			// Set IP Forwarding
-			fw := &ffdTestFirewaller{}
-			err = setupIPv4Forwarding(fw, wantFFD)
+			ffd := &ffDropper{}
+			err := setupIPv4Forwarding(ffd, wantFFD)
 			assert.NilError(t, err)
 
 			// Check what the firewaller was told.
-			if wantFFD {
-				assert.Check(t, is.Equal(fw.ffd, firewaller.IPv4))
-			} else {
-				var noVer firewaller.IPVersion
-				assert.Check(t, is.Equal(fw.ffd, noVer))
-			}
+			assert.Check(t, is.Equal(ffd.ffDrop4, wantFFD))
+			assert.Check(t, !ffd.ffDrop6)
 
 			// Read new setting
 			procSetting, err := os.ReadFile(ipv4ForwardConf)
@@ -65,23 +61,15 @@ func TestSetupIP6Forwarding(t *testing.T) {
 
 	for _, wantFFD := range []bool{true, false} {
 		t.Run(fmt.Sprintf("wantFFD=%v", wantFFD), func(t *testing.T) {
-			_, err := configureIPForwarding(ipv6ForwardConfDefault, '0')
-			assert.NilError(t, err)
-			_, err = configureIPForwarding(ipv6ForwardConfAll, '0')
-			assert.NilError(t, err)
+			// Disable IP Forwarding if enabled
+			setForwarding(t, '0')
 
 			// Set IP Forwarding
-			fw := &ffdTestFirewaller{}
-			err = setupIPv6Forwarding(fw, wantFFD)
+			ffd := &ffDropper{}
+			err := setupIPv6Forwarding(ffd, wantFFD)
 			assert.NilError(t, err)
-
-			// Check what the firewaller was told.
-			if wantFFD {
-				assert.Check(t, is.Equal(fw.ffd, firewaller.IPv6))
-			} else {
-				var noVer firewaller.IPVersion
-				assert.Check(t, is.Equal(fw.ffd, noVer))
-			}
+			assert.Check(t, !ffd.ffDrop4)
+			assert.Check(t, is.Equal(ffd.ffDrop6, wantFFD))
 
 			// Read new setting
 			procSetting, err := os.ReadFile(ipv6ForwardConfDefault)
@@ -93,3 +81,30 @@ func TestSetupIP6Forwarding(t *testing.T) {
 		})
 	}
 }
+
+func TestCheckForwarding(t *testing.T) {
+	defer netnsutils.SetupTestOSContext(t)()
+
+	setForwarding(t, '0')
+	err := checkIPv4Forwarding()
+	assert.Check(t, is.ErrorContains(err, "IPv4 forwarding is disabled"))
+	err = checkIPv6Forwarding()
+	assert.Check(t, is.ErrorContains(err, "IPv6 global forwarding is disabled"))
+
+	setForwarding(t, '1')
+	err = checkIPv4Forwarding()
+	assert.Check(t, err)
+	err = checkIPv6Forwarding()
+	assert.Check(t, err)
+}
+
+func setForwarding(t *testing.T, val byte) {
+	for _, sysctl := range []string{
+		ipv4ForwardConf,
+		ipv6ForwardConfDefault,
+		ipv6ForwardConfAll,
+	} {
+		err := os.WriteFile(sysctl, []byte{val, '\n'}, 0o644)
+		assert.NilError(t, err)
+	}
+}
diff --git a/daemon/libnetwork/iptables/iptables.go b/daemon/libnetwork/iptables/iptables.go
index f2d473cc93..dd46c8ef06 100644
--- a/daemon/libnetwork/iptables/iptables.go
+++ b/daemon/libnetwork/iptables/iptables.go
@@ -3,6 +3,7 @@
 package iptables
 
 import (
+	"bytes"
 	"context"
 	"errors"
 	"fmt"
@@ -411,6 +412,16 @@ func (iptable IPTable) SetDefaultPolicy(table Table, chain string, policy Policy
 	return nil
 }
 
+// HasPolicy returns true if the chain exists and has the given policy.
+func (iptable IPTable) HasPolicy(table Table, chain string, policy Policy) bool {
+	out, err := iptable.Raw("-t", string(table), "-L", chain)
+	if err != nil {
+		return false
+	}
+	firstLine, _, _ := bytes.Cut(out, []byte("\n"))
+	return strings.Contains(string(firstLine), "policy "+string(policy))
+}
+
 // AddReturnRule adds a return rule for the chain in the filter table
 func (iptable IPTable) AddReturnRule(table Table, chain string) error {
 	if iptable.Exists(table, chain, "-j", "RETURN") {
diff --git a/hack/make/.integration-daemon-start b/hack/make/.integration-daemon-start
index 78f056356f..76d2efecdf 100644
--- a/hack/make/.integration-daemon-start
+++ b/hack/make/.integration-daemon-start
@@ -67,6 +67,13 @@ fi
 
 dockerd="dockerd"
 
+# When running with the nftables backend, dockerd will not enable IP forwarding (by default, it
+# will error on network creation if forwarding is not enabled).
+if [ "$DOCKER_FIREWALL_BACKEND" = "nftables" ]; then
+	sysctl -w net.ipv4.ip_forward=1 > /dev/null
+	sysctl -w net.ipv6.conf.all.forwarding=1 > /dev/null
+fi
+
 if [ -n "$DOCKER_ROOTLESS" ]; then
 	if [ -z "$TEST_SKIP_INTEGRATION_CLI" ]; then
 		echo >&2 '# DOCKER_ROOTLESS requires TEST_SKIP_INTEGRATION_CLI to be set'
diff --git a/integration/internal/testutils/networking/firewall.go b/integration/internal/testutils/networking/firewall.go
index c7ba4e48ce..0c03087fc3 100644
--- a/integration/internal/testutils/networking/firewall.go
+++ b/integration/internal/testutils/networking/firewall.go
@@ -1,7 +1,6 @@
 package networking
 
 import (
-	"fmt"
 	"os/exec"
 	"regexp"
 	"strings"
@@ -9,45 +8,29 @@ import (
 
 	"github.com/moby/moby/v2/testutil/daemon"
 	"gotest.tools/v3/assert"
+	is "gotest.tools/v3/assert/cmp"
 	"gotest.tools/v3/icmd"
 	"gotest.tools/v3/poll"
 )
 
-const (
-	// The name of the bridge driver's nftables tables.
-	nftTable = "docker-bridges"
-	// The name of the filter-FORWARD chain in nftTable.
-	nftFFChain = "filter-FORWARD"
-)
-
 // Find the policy in, for example "Chain FORWARD (policy ACCEPT)".
 var rePolicy = regexp.MustCompile("policy ([A-Za-z]+)")
 
 // SetFilterForwardPolicies sets the default policy for the FORWARD chain in
-// the filter tables for both IPv4 and IPv6. The original policy is restored
-// using t.Cleanup().
+// the iptables filter tables for both IPv4 and IPv6. The original policy is
+// restored using t.Cleanup().
 //
 // There's only one filter-FORWARD policy, so this won't behave well if used by
 // tests running in parallel in a single network namespace that expect different
 // behaviour.
-func SetFilterForwardPolicies(t *testing.T, firewallBackend string, policy string) {
-	t.Helper()
-	if strings.HasPrefix(firewallBackend, "iptables") {
-		setIptablesFFP(t, policy)
-		return
-	}
-	if strings.HasPrefix(firewallBackend, "nftables") {
-		setNftablesFFP(t, policy)
-		return
-	}
-	t.Fatalf("unknown firewall backend %s", firewallBackend)
-}
-
-func setIptablesFFP(t *testing.T, policy string) {
+func SetFilterForwardPolicies(t *testing.T, policy string) {
 	t.Helper()
 	for _, iptablesCmd := range []string{"iptables", "ip6tables"} {
-		origPolicy, err := getChainPolicy(t, exec.Command(iptablesCmd, "-L", "FORWARD"))
-		assert.NilError(t, err, "failed to get iptables policy")
+		out, err := exec.Command(iptablesCmd, "-L", "FORWARD").Output()
+		assert.NilError(t, err, "failed to get %s policy", iptablesCmd)
+		opMatch := rePolicy.FindSubmatch(out)
+		assert.Assert(t, is.Len(opMatch, 2), "searching for policy: %w", err)
+		origPolicy := string(opMatch[1])
 		if origPolicy == policy {
 			continue
 		}
@@ -62,42 +45,6 @@ func setIptablesFFP(t *testing.T, policy string) {
 	}
 }
 
-func setNftablesFFP(t *testing.T, policy string) {
-	t.Helper()
-	policy = strings.ToLower(policy)
-	for _, family := range []string{"ip", "ip6"} {
-		origPolicy, err := getChainPolicy(t, exec.Command("nft", "list", "chain", family, nftTable, nftFFChain))
-		assert.NilError(t, err, "failed to get nftables policy")
-		if origPolicy == policy {
-			continue
-		}
-		cmd := func(p string) *exec.Cmd {
-			return exec.Command("nft", "add", "chain", family, nftTable, nftFFChain, "{", "policy", p, ";", "}")
-		}
-		if err := cmd(policy).Run(); err != nil {
-			t.Fatalf("Failed to set %s filter-FORWARD policy: %v", family, err)
-		}
-		t.Cleanup(func() {
-			if err := cmd(origPolicy).Run(); err != nil {
-				t.Logf("Failed to restore %s filter-FORWARD policy: %v", family, err)
-			}
-		})
-	}
-}
-
-func getChainPolicy(t *testing.T, cmd *exec.Cmd) (string, error) {
-	t.Helper()
-	out, err := cmd.Output()
-	if err != nil {
-		return "", fmt.Errorf("getting policy: %w", err)
-	}
-	opMatch := rePolicy.FindSubmatch(out)
-	if len(opMatch) != 2 {
-		return "", fmt.Errorf("searching for policy: %w", err)
-	}
-	return string(opMatch[1]), nil
-}
-
 // FirewalldRunning returns true if "firewall-cmd --state" reports "running".
 func FirewalldRunning() bool {
 	state, err := exec.Command("firewall-cmd", "--state").CombinedOutput()
diff --git a/integration/internal/testutils/networking/l3_segment_linux.go b/integration/internal/testutils/networking/l3_segment_linux.go
index 26b4a69659..eb923eff2a 100644
--- a/integration/internal/testutils/networking/l3_segment_linux.go
+++ b/integration/internal/testutils/networking/l3_segment_linux.go
@@ -77,6 +77,8 @@ func (l3 *L3Segment) AddHost(t *testing.T, hostname, nsName, ifname string, addr
 	l3.bridge.MustRun(t, "ip", "link", "set", hostname, "up", "master", l3.bridge.Iface)
 	host.MustRun(t, "ip", "link", "set", host.Iface, "up")
 	host.MustRun(t, "ip", "link", "set", "lo", "up")
+	host.MustRun(t, "sysctl", "-w", "net.ipv4.ip_forward=1")
+	host.MustRun(t, "sysctl", "-w", "net.ipv6.conf.all.forwarding=1")
 
 	for _, addr := range addrs {
 		host.MustRun(t, "ip", "addr", "add", addr.String(), "dev", host.Iface, "nodad")
diff --git a/integration/network/bridge/bridge_linux_test.go b/integration/network/bridge/bridge_linux_test.go
index 85a89bac13..671d744479 100644
--- a/integration/network/bridge/bridge_linux_test.go
+++ b/integration/network/bridge/bridge_linux_test.go
@@ -246,6 +246,8 @@ func TestIPRangeAt64BitLimit(t *testing.T) {
 func TestFilterForwardPolicy(t *testing.T) {
 	skip.If(t, testEnv.IsRootless, "rootless has its own netns")
 	skip.If(t, networking.FirewalldRunning(), "can't use firewalld in host netns to add rules in L3Segment")
+	skip.If(t, strings.HasPrefix(testEnv.FirewallBackendDriver(), "nftables"), "no policy is set for nftables")
+
 	ctx := setupTest(t)
 
 	// Set up a netns for each test to avoid sysctl and iptables pollution.
@@ -305,30 +307,17 @@ func TestFilterForwardPolicy(t *testing.T) {
 			)
 			host := l3.Hosts[hostname]
 
-			getFwdPolicy := func(usingNftables bool, fam string) string {
+			getFwdPolicy := func(cmd string) string {
 				t.Helper()
-				if usingNftables {
-					out := host.MustRun(t, "nft", "list chain "+fam+" docker-bridges filter-FORWARD")
-					if strings.Contains(out, "policy accept") {
-						return "ACCEPT"
-					}
-					if strings.Contains(out, "policy drop") {
-						return "DROP"
-					}
-					t.Fatalf("Failed to determine nftables filter-FORWARD policy: %s", out)
-					return ""
-				} else {
-					cmd := fam + "tables"
-					out := host.MustRun(t, cmd, "-S", "FORWARD")
-					if strings.HasPrefix(out, "-P FORWARD ACCEPT") {
-						return "ACCEPT"
-					}
-					if strings.HasPrefix(out, "-P FORWARD DROP") {
-						return "DROP"
-					}
-					t.Fatalf("Failed to determine %s FORWARD policy: %s", cmd, out)
-					return ""
+				out := host.MustRun(t, cmd, "-S", "FORWARD")
+				if strings.HasPrefix(out, "-P FORWARD ACCEPT") {
+					return "ACCEPT"
 				}
+				if strings.HasPrefix(out, "-P FORWARD DROP") {
+					return "DROP"
+				}
+				t.Fatalf("Failed to determine %s FORWARD policy: %s", cmd, out)
+				return ""
 			}
 
 			type sysctls struct{ v4, v6def, v6all string }
@@ -354,22 +343,21 @@ func TestFilterForwardPolicy(t *testing.T) {
 				d.StartWithBusybox(ctx, t, tc.daemonArgs...)
 				t.Cleanup(func() { d.Stop(t) })
 			})
-			usingNftables := d.FirewallBackendDriver(t) == "nftables"
 			c := d.NewClientT(t)
 			t.Cleanup(func() { c.Close() })
 
 			// If necessary, the IPv4 policy should have been updated when the default bridge network was created.
-			assert.Check(t, is.Equal(getFwdPolicy(usingNftables, "ip"), tc.expPolicy))
+			assert.Check(t, is.Equal(getFwdPolicy("iptables"), tc.expPolicy))
 			// IPv6 policy should not have been updated yet.
-			assert.Check(t, is.Equal(getFwdPolicy(usingNftables, "ip6"), "ACCEPT"))
+			assert.Check(t, is.Equal(getFwdPolicy("ip6tables"), "ACCEPT"))
 			assert.Check(t, is.Equal(getSysctls(), sysctls{tc.expForwarding, tc.initForwarding, tc.initForwarding}))
 
 			// If necessary, creating an IPv6 network should update the sysctls and policy.
 			const netName = "testnetffp"
 			network.CreateNoError(ctx, t, c, netName, network.WithIPv6())
 			t.Cleanup(func() { network.RemoveNoError(ctx, t, c, netName) })
-			assert.Check(t, is.Equal(getFwdPolicy(usingNftables, "ip"), tc.expPolicy))
-			assert.Check(t, is.Equal(getFwdPolicy(usingNftables, "ip6"), tc.expPolicy))
+			assert.Check(t, is.Equal(getFwdPolicy("iptables"), tc.expPolicy))
+			assert.Check(t, is.Equal(getFwdPolicy("ip6tables"), tc.expPolicy))
 			assert.Check(t, is.Equal(getSysctls(), sysctls{tc.expForwarding, tc.expForwarding, tc.expForwarding}))
 		})
 	}
diff --git a/integration/networking/bridge_linux_test.go b/integration/networking/bridge_linux_test.go
index 47ec967f97..919d5d0871 100644
--- a/integration/networking/bridge_linux_test.go
+++ b/integration/networking/bridge_linux_test.go
@@ -358,7 +358,6 @@ func TestBridgeINCRouted(t *testing.T) {
 	d := daemon.New(t)
 	d.StartWithBusybox(ctx, t)
 	t.Cleanup(func() { d.Stop(t) })
-	firewallBackend := d.FirewallBackendDriver(t)
 
 	c := d.NewClientT(t)
 	t.Cleanup(func() { c.Close() })
@@ -457,10 +456,12 @@ func TestBridgeINCRouted(t *testing.T) {
 		},
 	}
 
-	for _, fwdPolicy := range []string{"ACCEPT", "DROP"} {
-		networking.SetFilterForwardPolicies(t, firewallBackend, fwdPolicy)
+	runTests := func(testName, policy string) {
 		networking.FirewalldReload(t, d)
-		t.Run(fwdPolicy, func(t *testing.T) {
+		t.Run(testName, func(t *testing.T) {
+			if policy != "" {
+				networking.SetFilterForwardPolicies(t, policy)
+			}
 			for _, tc := range testcases {
 				t.Run(tc.name+"/v4/ping", func(t *testing.T) {
 					t.Parallel()
@@ -497,6 +498,13 @@ func TestBridgeINCRouted(t *testing.T) {
 			}
 		})
 	}
+
+	if strings.HasPrefix(d.FirewallBackendDriver(t), "iptables") {
+		runTests("iptables-ACCEPT", "ACCEPT")
+		runTests("iptables-DROP", "DROP")
+	} else {
+		runTests("nftables", "")
+	}
 }
 
 // TestAccessToPublishedPort checks that a container in one network can
diff --git a/integration/networking/port_mapping_linux_test.go b/integration/networking/port_mapping_linux_test.go
index 231258b4db..1993878d5e 100644
--- a/integration/networking/port_mapping_linux_test.go
+++ b/integration/networking/port_mapping_linux_test.go
@@ -648,7 +648,6 @@ func TestDirectRoutingOpenPorts(t *testing.T) {
 	d := daemon.New(t)
 	d.StartWithBusybox(ctx, t)
 	t.Cleanup(func() { d.Stop(t) })
-	firewallBackend := d.FirewallBackendDriver(t)
 
 	c := d.NewClientT(t)
 	t.Cleanup(func() { c.Close() })
@@ -770,9 +769,11 @@ func TestDirectRoutingOpenPorts(t *testing.T) {
 	// Run the ping and http tests in two parallel groups, rather than waiting for
 	// ping/http timeouts separately. (The iptables filter-FORWARD policy affects the
 	// whole host, so ACCEPT/DROP tests can't be parallelized).
-	for _, fwdPolicy := range []string{"ACCEPT", "DROP"} {
-		networking.SetFilterForwardPolicies(t, firewallBackend, fwdPolicy)
-		t.Run(fwdPolicy, func(t *testing.T) {
+	runTests := func(testName, policy string) {
+		t.Run(testName, func(t *testing.T) {
+			if policy != "" {
+				networking.SetFilterForwardPolicies(t, policy)
+			}
 			for gwMode := range networks {
 				t.Run(gwMode+"/v4/ping", func(t *testing.T) {
 					testPing(t, "ping", networks[gwMode].ipv4, expPingExit[gwMode])
@@ -795,6 +796,13 @@ func TestDirectRoutingOpenPorts(t *testing.T) {
 			}
 		})
 	}
+
+	if strings.HasPrefix(d.FirewallBackendDriver(t), "iptables") {
+		runTests("iptables-ACCEPT", "ACCEPT")
+		runTests("iptables-DROP", "DROP")
+	} else {
+		runTests("nftables", "")
+	}
 }
 
 func TestAcceptFwMark(t *testing.T) {