diff --git a/.changelog/15473.txt b/.changelog/15473.txt
new file mode 100644
index 000000000..7e8a6535b
--- /dev/null
+++ b/.changelog/15473.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+networking: Inject constraints on CNI plugins when using bridge networking
+```
diff --git a/client/allocrunner/networking_bridge_linux.go b/client/allocrunner/networking_bridge_linux.go
index 89b7b2cb0..908bba96f 100644
--- a/client/allocrunner/networking_bridge_linux.go
+++ b/client/allocrunner/networking_bridge_linux.go
@@ -148,7 +148,8 @@ func buildNomadBridgeNetConfig(b bridgeNetworkConfigurator) []byte {
 }
 
 // Update website/content/docs/networking/cni.mdx when the bridge configuration
-// is modified.
+// is modified. If CNI plugins are added or versions need to be updated for new
+// fields, add a new constraint to nomad/job_endpoint_hooks.go
 const nomadCNIConfigTemplate = `{
 	"cniVersion": "0.4.0",
 	"name": "nomad",
diff --git a/nomad/job_endpoint_hooks.go b/nomad/job_endpoint_hooks.go
index c58a5a00a..809958c38 100644
--- a/nomad/job_endpoint_hooks.go
+++ b/nomad/job_endpoint_hooks.go
@@ -15,13 +15,24 @@ import (
 	"golang.org/x/exp/maps"
 )
 
+// Node attributes acquired via fingerprinting.
 const (
 	attrVaultVersion      = `${attr.vault.version}`
 	attrConsulVersion     = `${attr.consul.version}`
 	attrNomadVersion      = `${attr.nomad.version}`
 	attrNomadServiceDisco = `${attr.nomad.service_discovery}`
+	attrBridgeCNI         = `${attr.plugins.cni.version.bridge}`
+	attrFirewallCNI       = `${attr.plugins.cni.version.firewall}`
+	attrHostLocalCNI      = `${attr.plugins.cni.version.host-local}`
+	attrLoopbackCNI       = `${attr.plugins.cni.version.loopback}`
+	attrPortMapCNI        = `${attr.plugins.cni.version.portmap}`
 )
 
+// cniMinVersion is the version expression for the minimum CNI version supported
+// for the CNI container-networking plugins. Support was added at v0.4.0, so
+// we set the minimum to that.
+const cniMinVersion = ">= 0.4.0"
+
 var (
 	// vaultConstraint is the implicit constraint added to jobs requesting a
 	// Vault token
@@ -78,6 +89,51 @@ var (
 		RTarget: "linux",
 		Operand: "=",
 	}
+
+	// cniBridgeConstraint is an implicit constraint added to jobs making use
+	// of bridge networking mode. This is one of the CNI plugins used to support
+	// bridge networking.
+	cniBridgeConstraint = &structs.Constraint{
+		LTarget: attrBridgeCNI,
+		RTarget: cniMinVersion,
+		Operand: structs.ConstraintSemver,
+	}
+
+	// cniFirewallConstraint is an implicit constraint added to jobs making use
+	// of bridge networking mode. This is one of the CNI plugins used to support
+	// bridge networking.
+	cniFirewallConstraint = &structs.Constraint{
+		LTarget: attrFirewallCNI,
+		RTarget: cniMinVersion,
+		Operand: structs.ConstraintSemver,
+	}
+
+	// cniHostLocalConstraint is an implicit constraint added to jobs making use
+	// of bridge networking mode. This is one of the CNI plugins used to support
+	// bridge networking.
+	cniHostLocalConstraint = &structs.Constraint{
+		LTarget: attrHostLocalCNI,
+		RTarget: cniMinVersion,
+		Operand: structs.ConstraintSemver,
+	}
+
+	// cniLoopbackConstraint is an implicit constraint added to jobs making use
+	// of bridge networking mode. This is one of the CNI plugins used to support
+	// bridge networking.
+	cniLoopbackConstraint = &structs.Constraint{
+		LTarget: attrLoopbackCNI,
+		RTarget: cniMinVersion,
+		Operand: structs.ConstraintSemver,
+	}
+
+	// cniPortMapConstraint is an implicit constraint added to jobs making use
+	// of bridge networking mode. This is one of the CNI plugins used to support
+	// bridge networking.
+	cniPortMapConstraint = &structs.Constraint{
+		LTarget: attrPortMapCNI,
+		RTarget: cniMinVersion,
+		Operand: structs.ConstraintSemver,
+	}
 )
 
 type admissionController interface {
@@ -192,12 +248,14 @@ func (jobImpliedConstraints) Mutate(j *structs.Job) (*structs.Job, []error, erro
 	// Identify which task groups are utilizing NUMA resources.
 	numaTaskGroups := j.RequiredNUMA()
 
+	bridgeNetworkingTaskGroups := j.RequiredBridgeNetwork()
+
 	// Hot path where none of our things require constraints.
 	//
 	// [UPDATE THIS] if you are adding a new constraint thing!
 	if len(signals) == 0 && len(vaultBlocks) == 0 &&
 		nativeServiceDisco.Empty() && len(consulServiceDisco) == 0 &&
-		numaTaskGroups.Empty() {
+		numaTaskGroups.Empty() && bridgeNetworkingTaskGroups.Empty() {
 		return j, nil, nil
 	}
 
@@ -254,6 +312,14 @@ func (jobImpliedConstraints) Mutate(j *structs.Job) (*structs.Job, []error, erro
 				}
 			}
 		}
+
+		if bridgeNetworkingTaskGroups.Contains(tg.Name) {
+			mutateConstraint(constraintMatcherLeft, tg, cniBridgeConstraint)
+			mutateConstraint(constraintMatcherLeft, tg, cniFirewallConstraint)
+			mutateConstraint(constraintMatcherLeft, tg, cniHostLocalConstraint)
+			mutateConstraint(constraintMatcherLeft, tg, cniLoopbackConstraint)
+			mutateConstraint(constraintMatcherLeft, tg, cniPortMapConstraint)
+		}
 	}
 
 	return j, nil, nil
diff --git a/nomad/job_endpoint_hooks_test.go b/nomad/job_endpoint_hooks_test.go
index aaf8b7deb..8b73cc7f9 100644
--- a/nomad/job_endpoint_hooks_test.go
+++ b/nomad/job_endpoint_hooks_test.go
@@ -1160,6 +1160,40 @@ func Test_jobImpliedConstraints_Mutate(t *testing.T) {
 			expectedOutputWarnings: nil,
 			expectedOutputError:    nil,
 		},
+		{
+			inputJob: &structs.Job{
+				Name: "example",
+				TaskGroups: []*structs.TaskGroup{
+					{
+						Name: "group-with-bridge",
+						Networks: []*structs.NetworkResource{
+							{Mode: "bridge"},
+						},
+					},
+				},
+			},
+			expectedOutputJob: &structs.Job{
+				Name: "example",
+				TaskGroups: []*structs.TaskGroup{
+					{
+						Name: "group-with-bridge",
+						Networks: []*structs.NetworkResource{
+							{Mode: "bridge"},
+						},
+						Constraints: []*structs.Constraint{
+							cniBridgeConstraint,
+							cniFirewallConstraint,
+							cniHostLocalConstraint,
+							cniLoopbackConstraint,
+							cniPortMapConstraint,
+						},
+					},
+				},
+			},
+			expectedOutputWarnings: nil,
+			expectedOutputError:    nil,
+			name:                   "task group with bridge network",
+		},
 	}
 
 	for _, tc := range testCases {
diff --git a/nomad/structs/job.go b/nomad/structs/job.go
index b356dade7..a064c5dc3 100644
--- a/nomad/structs/job.go
+++ b/nomad/structs/job.go
@@ -132,3 +132,15 @@ func (j *Job) RequiredNUMA() set.Collection[string] {
 	}
 	return result
 }
+
+// RequiredBridgeNetwork identifies which task groups, if any, within the job
+// contain networks requesting bridge networking.
+func (j *Job) RequiredBridgeNetwork() set.Collection[string] {
+	result := set.New[string](len(j.TaskGroups))
+	for _, tg := range j.TaskGroups {
+		if tg.Networks.Modes().Contains("bridge") {
+			result.Insert(tg.Name)
+		}
+	}
+	return result
+}
diff --git a/nomad/structs/structs.go b/nomad/structs/structs.go
index 8e1cc49a7..f58b0bc19 100644
--- a/nomad/structs/structs.go
+++ b/nomad/structs/structs.go
@@ -3006,6 +3006,13 @@ func (ns Networks) NetIndex(n *NetworkResource) int {
 	return -1
 }
 
+// Modes returns the set of network modes used by our NetworkResource blocks.
+func (ns Networks) Modes() *set.Set[string] {
+	return set.FromFunc(ns, func(nr *NetworkResource) string {
+		return nr.Mode
+	})
+}
+
 // RequestedDevice is used to request a device for a task.
 type RequestedDevice struct {
 	// Name is the request name. The possible values are as follows:
diff --git a/website/content/docs/upgrade/upgrade-specific.mdx b/website/content/docs/upgrade/upgrade-specific.mdx
index 87a039d50..e58a20ae0 100644
--- a/website/content/docs/upgrade/upgrade-specific.mdx
+++ b/website/content/docs/upgrade/upgrade-specific.mdx
@@ -14,12 +14,26 @@ their upgrades as a result of new features or changed behavior. This page is
 used to document those details separately from the standard upgrade flow.
 
 ## Nomad 1.8.0
+
+#### Deprecated Disconnect Fields
+
 Nomad 1.8.0 introduces a `disconnect` block meant to group all the configuration
-options related to disconnected client's and server's behavior, causing the 
-deprecation of the fileds `stop_after_client_disconnect`, `max_client_disconnect`
+options related to disconnected client's and server's behavior, causing the
+deprecation of the fields `stop_after_client_disconnect`, `max_client_disconnect`
 and `prevent_reschedule_on_lost`. This block also introduces new options for
 allocations reconciliation if the client regains connectivity.
 
+#### CNI Constraints
+
+In Nomad 1.8.0, jobs with `bridge` networking will have constraints added during
+job submit that require CNI plugins to be present on the node. Nodes have
+fingerprinted the available CNI plugins starting in Nomad 1.5.0.
+
+If you are upgrading from Nomad 1.5.0 or later to 1.8.0 or later, there's
+nothing additional for you to do. It's not recommended to skip more than 2
+versions of Nomad. But if you upgrade from earlier than 1.5.0 to 1.8.0 or later,
+you will need to ensure that clients have been upgraded before submitting any
+jobs that use `bridge` networking.
 
 #### Removal of `raw_exec` option `no_cgroups`