diff --git a/.changelog/24650.txt b/.changelog/24650.txt
new file mode 100644
index 00000000000..5efb4f2330e
--- /dev/null
+++ b/.changelog/24650.txt
@@ -0,0 +1,3 @@
+```release-note:bug
+networking: use a tmpfs location for the state of CNI IPAM plugin used by bridge mode, to fix a bug where allocations would fail to restore after host reboot
+```
diff --git a/client/allocrunner/cni/bridge.go b/client/allocrunner/cni/bridge.go
index 91b438b8e59..5889c2f510d 100644
--- a/client/allocrunner/cni/bridge.go
+++ b/client/allocrunner/cni/bridge.go
@@ -58,9 +58,10 @@ func NewNomadBridgeConflist(conf NomadBridgeConfig) Conflist {
 			ForceAddress: true,
 			HairpinMode:  conf.HairpinMode,
 			Ipam: IPAM{
-				Type:   "host-local",
-				Ranges: ipRanges,
-				Routes: ipRoutes,
+				Type:    "host-local",
+				Ranges:  ipRanges,
+				Routes:  ipRoutes,
+				DataDir: "/var/run/cni",
 			},
 		},
 		Firewall{
diff --git a/client/allocrunner/cni/plugins.go b/client/allocrunner/cni/plugins.go
index 091208ca3ba..f31ff9dd605 100644
--- a/client/allocrunner/cni/plugins.go
+++ b/client/allocrunner/cni/plugins.go
@@ -20,9 +20,10 @@ type Bridge struct {
 	Ipam         IPAM   `json:"ipam"`
 }
 type IPAM struct {
-	Type   string    `json:"type"`
-	Ranges [][]Range `json:"ranges"`
-	Routes []Route   `json:"routes"`
+	Type    string    `json:"type"`
+	Ranges  [][]Range `json:"ranges"`
+	Routes  []Route   `json:"routes"`
+	DataDir string    `json:"dataDir"`
 }
 type Range struct {
 	Subnet string `json:"subnet"`
diff --git a/client/allocrunner/test_fixtures/bad_input.conflist.json b/client/allocrunner/test_fixtures/bad_input.conflist.json
index f9c9be906ce..9b2bb2fc990 100644
--- a/client/allocrunner/test_fixtures/bad_input.conflist.json
+++ b/client/allocrunner/test_fixtures/bad_input.conflist.json
@@ -25,7 +25,8 @@
 					{
 						"dst": "0.0.0.0/0"
 					}
-				]
+				],
+				"dataDir": "/var/run/cni"
 			}
 		},
 		{
diff --git a/client/allocrunner/test_fixtures/consul-cni.conflist.json b/client/allocrunner/test_fixtures/consul-cni.conflist.json
index 3fe7b270edb..95b7a9c0058 100644
--- a/client/allocrunner/test_fixtures/consul-cni.conflist.json
+++ b/client/allocrunner/test_fixtures/consul-cni.conflist.json
@@ -25,7 +25,8 @@
 					{
 						"dst": "0.0.0.0/0"
 					}
-				]
+				],
+				"dataDir": "/var/run/cni"
 			}
 		},
 		{
diff --git a/client/allocrunner/test_fixtures/empty.conflist.json b/client/allocrunner/test_fixtures/empty.conflist.json
index 484feb44674..7ac34cdf404 100644
--- a/client/allocrunner/test_fixtures/empty.conflist.json
+++ b/client/allocrunner/test_fixtures/empty.conflist.json
@@ -25,7 +25,8 @@
 					{
 						"dst": "0.0.0.0/0"
 					}
-				]
+				],
+				"dataDir": "/var/run/cni"
 			}
 		},
 		{
diff --git a/client/allocrunner/test_fixtures/hairpin.conflist.json b/client/allocrunner/test_fixtures/hairpin.conflist.json
index 1e584c6c115..ba6f276472c 100644
--- a/client/allocrunner/test_fixtures/hairpin.conflist.json
+++ b/client/allocrunner/test_fixtures/hairpin.conflist.json
@@ -25,7 +25,8 @@
 					{
 						"dst": "0.0.0.0/0"
 					}
-				]
+				],
+				"dataDir": "/var/run/cni"
 			}
 		},
 		{
diff --git a/client/allocrunner/test_fixtures/ipv6.conflist.json b/client/allocrunner/test_fixtures/ipv6.conflist.json
index e71afdbe5a7..eb15ada4b12 100644
--- a/client/allocrunner/test_fixtures/ipv6.conflist.json
+++ b/client/allocrunner/test_fixtures/ipv6.conflist.json
@@ -33,7 +33,8 @@
 					{
 						"dst": "::/0"
 					}
-				]
+				],
+				"dataDir": "/var/run/cni"
 			}
 		},
 		{