diff --git a/.changelog/24658.txt b/.changelog/24658.txt
new file mode 100644
index 00000000000..f46da955490
--- /dev/null
+++ b/.changelog/24658.txt
@@ -0,0 +1,3 @@
+```release-note:bug
+networking: check network namespaces on Linux during client restarts and fail the allocation if an existing namespace is invalid
+```
diff --git a/client/allocrunner/network_hook.go b/client/allocrunner/network_hook.go
index 570943b3795..af72ba7df5a 100644
--- a/client/allocrunner/network_hook.go
+++ b/client/allocrunner/network_hook.go
@@ -142,11 +142,14 @@ func (h *networkHook) Prerun() error {
 		h.isolationSetter.SetNetworkIsolation(spec)
 	}
 
-	if created {
-		status, err := h.networkConfigurator.Setup(context.TODO(), h.alloc, spec)
+	if spec != nil {
+		status, err := h.networkConfigurator.Setup(context.TODO(), h.alloc, spec, created)
 		if err != nil {
 			return fmt.Errorf("failed to configure networking for alloc: %v", err)
 		}
+		if status == nil {
+			return nil // netns already existed and was correctly configured
+		}
 
 		// If the driver set the sandbox hostname label, then we will use that
 		// to set the HostsConfig.Hostname. Otherwise, identify the sandbox
diff --git a/client/allocrunner/networking.go b/client/allocrunner/networking.go
index e98af0b4f89..07a98660795 100644
--- a/client/allocrunner/networking.go
+++ b/client/allocrunner/networking.go
@@ -14,7 +14,7 @@ import (
 // NetworkConfigurator sets up and tears down the interfaces, routes, firewall
 // rules, etc for the configured networking mode of the allocation.
 type NetworkConfigurator interface {
-	Setup(context.Context, *structs.Allocation, *drivers.NetworkIsolationSpec) (*structs.AllocNetworkStatus, error)
+	Setup(context.Context, *structs.Allocation, *drivers.NetworkIsolationSpec, bool) (*structs.AllocNetworkStatus, error)
 	Teardown(context.Context, *structs.Allocation, *drivers.NetworkIsolationSpec) error
 }
 
@@ -23,7 +23,7 @@ type NetworkConfigurator interface {
 // require further configuration
 type hostNetworkConfigurator struct{}
 
-func (h *hostNetworkConfigurator) Setup(context.Context, *structs.Allocation, *drivers.NetworkIsolationSpec) (*structs.AllocNetworkStatus, error) {
+func (h *hostNetworkConfigurator) Setup(context.Context, *structs.Allocation, *drivers.NetworkIsolationSpec, bool) (*structs.AllocNetworkStatus, error) {
 	return nil, nil
 }
 func (h *hostNetworkConfigurator) Teardown(context.Context, *structs.Allocation, *drivers.NetworkIsolationSpec) error {
@@ -41,10 +41,10 @@ type synchronizedNetworkConfigurator struct {
 	nc NetworkConfigurator
 }
 
-func (s *synchronizedNetworkConfigurator) Setup(ctx context.Context, allocation *structs.Allocation, spec *drivers.NetworkIsolationSpec) (*structs.AllocNetworkStatus, error) {
+func (s *synchronizedNetworkConfigurator) Setup(ctx context.Context, allocation *structs.Allocation, spec *drivers.NetworkIsolationSpec, created bool) (*structs.AllocNetworkStatus, error) {
 	networkingGlobalMutex.Lock()
 	defer networkingGlobalMutex.Unlock()
-	return s.nc.Setup(ctx, allocation, spec)
+	return s.nc.Setup(ctx, allocation, spec, created)
 }
 
 func (s *synchronizedNetworkConfigurator) Teardown(ctx context.Context, allocation *structs.Allocation, spec *drivers.NetworkIsolationSpec) error {
diff --git a/client/allocrunner/networking_bridge_linux.go b/client/allocrunner/networking_bridge_linux.go
index 63a11c8f093..1204837b0dd 100644
--- a/client/allocrunner/networking_bridge_linux.go
+++ b/client/allocrunner/networking_bridge_linux.go
@@ -120,12 +120,12 @@ func (b *bridgeNetworkConfigurator) ensureForwardingRules() error {
 }
 
 // Setup calls the CNI plugins with the add action
-func (b *bridgeNetworkConfigurator) Setup(ctx context.Context, alloc *structs.Allocation, spec *drivers.NetworkIsolationSpec) (*structs.AllocNetworkStatus, error) {
+func (b *bridgeNetworkConfigurator) Setup(ctx context.Context, alloc *structs.Allocation, spec *drivers.NetworkIsolationSpec, created bool) (*structs.AllocNetworkStatus, error) {
 	if err := b.ensureForwardingRules(); err != nil {
 		return nil, fmt.Errorf("failed to initialize table forwarding rules: %v", err)
 	}
 
-	return b.cni.Setup(ctx, alloc, spec)
+	return b.cni.Setup(ctx, alloc, spec, created)
 }
 
 // Teardown calls the CNI plugins with the delete action
diff --git a/client/allocrunner/networking_cni.go b/client/allocrunner/networking_cni.go
index 1c877fbe2ff..30d73c0d6f3 100644
--- a/client/allocrunner/networking_cni.go
+++ b/client/allocrunner/networking_cni.go
@@ -139,7 +139,8 @@ func addNomadWorkloadCNIArgs(logger log.Logger, alloc *structs.Allocation, cniAr
 }
 
 // Setup calls the CNI plugins with the add action
-func (c *cniNetworkConfigurator) Setup(ctx context.Context, alloc *structs.Allocation, spec *drivers.NetworkIsolationSpec) (*structs.AllocNetworkStatus, error) {
+func (c *cniNetworkConfigurator) Setup(ctx context.Context, alloc *structs.Allocation, spec *drivers.NetworkIsolationSpec, created bool) (*structs.AllocNetworkStatus, error) {
+
 	if err := c.ensureCNIInitialized(); err != nil {
 		return nil, fmt.Errorf("cni not initialized: %w", err)
 	}
@@ -171,6 +172,16 @@ func (c *cniNetworkConfigurator) Setup(ctx context.Context, alloc *structs.Alloc
 		cniArgs[ConsulIPTablesConfigEnvVar] = string(iptablesCfg)
 	}
 
+	if !created {
+		err := c.cni.Check(ctx, alloc.ID, spec.Path,
+			c.nsOpts.withCapabilityPortMap(portMaps.ports),
+			c.nsOpts.withArgs(cniArgs),
+		)
+		// return early: either the netns is ok or we need to start the alloc
+		// over anyways
+		return nil, err
+	}
+
 	// Depending on the version of bridge cni plugin used, a known race could occure
 	// where two alloc attempt to create the nomad bridge at the same time, resulting
 	// in one of them to fail. This rety attempts to overcome those erroneous failures.
diff --git a/client/allocrunner/networking_cni_test.go b/client/allocrunner/networking_cni_test.go
index 798d641adb4..f76f2b2462e 100644
--- a/client/allocrunner/networking_cni_test.go
+++ b/client/allocrunner/networking_cni_test.go
@@ -296,7 +296,7 @@ func TestSetup(t *testing.T) {
 			}
 
 			// method under test
-			result, err := c.Setup(context.Background(), alloc, spec)
+			result, err := c.Setup(context.Background(), alloc, spec, true)
 			if tc.expectErr == "" {
 				must.NoError(t, err)
 				must.Eq(t, tc.expectResult, result)