diff --git a/.changelog/3531.txt b/.changelog/3531.txt
new file mode 100644
index 0000000000..cd61ff3ce2
--- /dev/null
+++ b/.changelog/3531.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+api-gateway: Apply `connectInject.initContainer.resources` to the init container for API gateway Pods.
+```
diff --git a/control-plane/api-gateway/common/helm_config.go b/control-plane/api-gateway/common/helm_config.go
index 7ce8e0778a..9b0ab1d7e8 100644
--- a/control-plane/api-gateway/common/helm_config.go
+++ b/control-plane/api-gateway/common/helm_config.go
@@ -6,6 +6,8 @@ package common
 import (
 	"strings"
 	"time"
+
+	v1 "k8s.io/api/core/v1"
 )
 
 const componentAuthMethod = "k8s-component-auth-method"
@@ -40,6 +42,8 @@ type HelmConfig struct {
 	// MapPrivilegedServicePorts is the value which Consul will add to privileged container port values (ports < 1024)
 	// defined on a Gateway.
 	MapPrivilegedServicePorts int
+
+	InitContainerResources *v1.ResourceRequirements
 }
 
 type ConsulConfig struct {
diff --git a/control-plane/api-gateway/gatekeeper/gatekeeper_test.go b/control-plane/api-gateway/gatekeeper/gatekeeper_test.go
index 72bf6aeabc..8e212344b5 100644
--- a/control-plane/api-gateway/gatekeeper/gatekeeper_test.go
+++ b/control-plane/api-gateway/gatekeeper/gatekeeper_test.go
@@ -15,6 +15,7 @@ import (
 	corev1 "k8s.io/api/core/v1"
 	rbac "k8s.io/api/rbac/v1"
 	k8serrors "k8s.io/apimachinery/pkg/api/errors"
+	"k8s.io/apimachinery/pkg/api/resource"
 	metav1 "k8s.io/apimachinery/pkg/apis/meta/v1"
 	"k8s.io/apimachinery/pkg/runtime"
 	"k8s.io/apimachinery/pkg/types"
@@ -109,6 +110,16 @@ func TestUpsert(t *testing.T) {
 			},
 			helmConfig: common.HelmConfig{
 				ImageDataplane: dataplaneImage,
+				InitContainerResources: &corev1.ResourceRequirements{
+					Limits: corev1.ResourceList{
+						corev1.ResourceCPU:    requireQuantity(t, "100m"),
+						corev1.ResourceMemory: requireQuantity(t, "2Gi"),
+					},
+					Requests: corev1.ResourceList{
+						corev1.ResourceCPU:    requireQuantity(t, "100m"),
+						corev1.ResourceMemory: requireQuantity(t, "2Gi"),
+					},
+				},
 			},
 			initialResources: resources{},
 			finalResources: resources{
@@ -764,7 +775,7 @@ func TestUpsert(t *testing.T) {
 
 			err := gatekeeper.Upsert(context.Background(), tc.gateway, tc.gatewayClassConfig, tc.helmConfig)
 			require.NoError(t, err)
-			require.NoError(t, validateResourcesExist(t, client, tc.finalResources))
+			require.NoError(t, validateResourcesExist(t, client, tc.helmConfig, tc.finalResources))
 		})
 	}
 }
@@ -953,7 +964,7 @@ func TestDelete(t *testing.T) {
 				Name:      tc.gateway.Name,
 			})
 			require.NoError(t, err)
-			require.NoError(t, validateResourcesExist(t, client, tc.finalResources))
+			require.NoError(t, validateResourcesExist(t, client, tc.helmConfig, tc.finalResources))
 			require.NoError(t, validateResourcesAreDeleted(t, client, tc.initialResources))
 		})
 	}
@@ -983,7 +994,7 @@ func joinResources(resources resources) (objs []client.Object) {
 	return objs
 }
 
-func validateResourcesExist(t *testing.T, client client.Client, resources resources) error {
+func validateResourcesExist(t *testing.T, client client.Client, helmConfig common.HelmConfig, resources resources) error {
 	t.Helper()
 
 	for _, expected := range resources.deployments {
@@ -1012,6 +1023,21 @@ func validateResourcesExist(t *testing.T, client client.Client, resources resour
 		require.Equal(t, expected.Spec.Template.ObjectMeta.Annotations, actual.Spec.Template.ObjectMeta.Annotations)
 		require.Equal(t, expected.Spec.Template.ObjectMeta.Labels, actual.Spec.Template.Labels)
 
+		// Ensure there is an init container
+		hasInitContainer := false
+		for _, container := range actual.Spec.Template.Spec.InitContainers {
+			if container.Name == injectInitContainerName {
+				hasInitContainer = true
+
+				// If the Helm config specifies init container resources, verify they are set
+				if helmConfig.InitContainerResources != nil {
+					assert.Equal(t, helmConfig.InitContainerResources.Limits, container.Resources.Limits)
+					assert.Equal(t, helmConfig.InitContainerResources.Requests, container.Resources.Requests)
+				}
+			}
+		}
+		assert.True(t, hasInitContainer)
+
 		// Ensure there is a consul-dataplane container dropping ALL capabilities, adding
 		// back the NET_BIND_SERVICE capability, and establishing a read-only root filesystem
 		hasDataplaneContainer := false
@@ -1349,3 +1375,9 @@ func configureServiceAccount(name, namespace string, labels map[string]string, r
 		},
 	}
 }
+
+func requireQuantity(t *testing.T, v string) resource.Quantity {
+	quantity, err := resource.ParseQuantity(v)
+	require.NoError(t, err)
+	return quantity
+}
diff --git a/control-plane/api-gateway/gatekeeper/init.go b/control-plane/api-gateway/gatekeeper/init.go
index f3d4ad1f95..1d57123fed 100644
--- a/control-plane/api-gateway/gatekeeper/init.go
+++ b/control-plane/api-gateway/gatekeeper/init.go
@@ -11,9 +11,10 @@ import (
 
 	corev1 "k8s.io/api/core/v1"
 
+	"k8s.io/utils/pointer"
+
 	"github.com/hashicorp/consul-k8s/control-plane/api-gateway/common"
 	"github.com/hashicorp/consul-k8s/control-plane/namespaces"
-	"k8s.io/utils/pointer"
 )
 
 const (
@@ -168,6 +169,10 @@ func initContainer(config common.HelmConfig, name, namespace string) (corev1.Con
 			})
 	}
 
+	if config.InitContainerResources != nil {
+		container.Resources = *config.InitContainerResources
+	}
+
 	// Openshift Assigns the security context for us, do not enable if it is enabled.
 	if !config.EnableOpenShift {
 		container.SecurityContext = &corev1.SecurityContext{
diff --git a/control-plane/subcommand/inject-connect/v1controllers.go b/control-plane/subcommand/inject-connect/v1controllers.go
index f717b873b0..0081935199 100644
--- a/control-plane/subcommand/inject-connect/v1controllers.go
+++ b/control-plane/subcommand/inject-connect/v1controllers.go
@@ -128,6 +128,7 @@ func (c *Command) configureV1Controllers(ctx context.Context, mgr manager.Manage
 			ConsulTLSServerName:        c.consul.TLSServerName,
 			ConsulPartition:            c.consul.Partition,
 			ConsulCACert:               string(c.caCertPem),
+			InitContainerResources:     &c.initContainerResources,
 		},
 		AllowK8sNamespacesSet:   allowK8sNamespaces,
 		DenyK8sNamespacesSet:    denyK8sNamespaces,