diff --git a/.changelog/25871.txt b/.changelog/25871.txt
new file mode 100644
index 000000000..e8e2a8241
--- /dev/null
+++ b/.changelog/25871.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+identity: Allow ACL policies to be applied to a namespace
+```
diff --git a/command/acl_policy_apply.go b/command/acl_policy_apply.go
index 1ec5cc105..6a396e222 100644
--- a/command/acl_policy_apply.go
+++ b/command/acl_policy_apply.go
@@ -35,14 +35,13 @@ Apply Options:
   -description
     Specifies a human readable description for the policy.
 
+  -namespace
+    Attaches the policy to the specified namespace.
+
   -job
     Attaches the policy to the specified job. Requires that -namespace is
     also set.
 
-  -namespace
-    Attaches the policy to the specified namespace. Requires that -job is
-    also set.
-
   -group
     Attaches the policy to the specified task group. Requires that -namespace
     and -job are also set.
diff --git a/nomad/auth/auth.go b/nomad/auth/auth.go
index a2d88a507..95a4fed7d 100644
--- a/nomad/auth/auth.go
+++ b/nomad/auth/auth.go
@@ -641,5 +641,23 @@ func (s *Authenticator) ResolvePoliciesForClaims(claims *structs.IdentityClaims)
 		}
 	}
 
+	iter, err = snap.ACLPolicyByNamespace(nil, alloc.Namespace)
+	if err != nil {
+		return nil, err
+	}
+	for {
+		raw := iter.Next()
+		if raw == nil {
+			break
+		}
+
+		policy := raw.(*structs.ACLPolicy)
+		if policy.JobACL == nil {
+			continue
+		}
+
+		policies = append(policies, policy)
+	}
+
 	return policies, nil
 }
diff --git a/nomad/auth/auth_test.go b/nomad/auth/auth_test.go
index 9be3bb78a..5de234474 100644
--- a/nomad/auth/auth_test.go
+++ b/nomad/auth/auth_test.go
@@ -1109,6 +1109,18 @@ func TestResolveClaims(t *testing.T) {
 		JobID:     claims.JobID,
 	}
 
+	// policy for namespace
+	policy8 := mock.ACLPolicy()
+	policy8.JobACL = &structs.JobACL{
+		Namespace: claims.Namespace,
+	}
+
+	// policy for different namespace
+	policy9 := mock.ACLPolicy()
+	policy9.JobACL = &structs.JobACL{
+		Namespace: "another",
+	}
+
 	aclObj, err := auth.resolveClaims(claims)
 	must.Nil(t, aclObj)
 	must.EqError(t, err, "allocation does not exist")
@@ -1127,7 +1139,7 @@ func TestResolveClaims(t *testing.T) {
 	// Add the policies
 	index++
 	err = auth.getState().UpsertACLPolicies(structs.MsgTypeTestSetup, index, []*structs.ACLPolicy{
-		policy0, policy1, policy2, policy3, policy4, policy5, policy6, policy7})
+		policy0, policy1, policy2, policy3, policy4, policy5, policy6, policy7, policy8, policy9})
 	must.NoError(t, err)
 
 	// Re-resolve and check that the resulting ACL looks reasonable
@@ -1146,8 +1158,8 @@ func TestResolveClaims(t *testing.T) {
 
 	policies, err := auth.ResolvePoliciesForClaims(claims)
 	must.NoError(t, err)
-	must.Len(t, 3, policies)
-	must.SliceContainsAll(t, policies, []*structs.ACLPolicy{policy1, policy2, policy3})
+	must.Len(t, 4, policies)
+	must.SliceContainsAll(t, policies, []*structs.ACLPolicy{policy1, policy2, policy3, policy8})
 
 	// Check the dispatch claims
 	aclObj3, err := auth.resolveClaims(dispatchClaims)
@@ -1157,8 +1169,8 @@ func TestResolveClaims(t *testing.T) {
 
 	dispatchPolicies, err := auth.ResolvePoliciesForClaims(dispatchClaims)
 	must.NoError(t, err)
-	must.Len(t, 3, dispatchPolicies)
-	must.SliceContainsAll(t, dispatchPolicies, []*structs.ACLPolicy{policy1, policy2, policy3})
+	must.Len(t, 4, dispatchPolicies)
+	must.SliceContainsAll(t, dispatchPolicies, []*structs.ACLPolicy{policy1, policy2, policy3, policy8})
 
 }
 
diff --git a/nomad/state/schema.go b/nomad/state/schema.go
index 8337d312a..021e7660e 100644
--- a/nomad/state/schema.go
+++ b/nomad/state/schema.go
@@ -907,10 +907,10 @@ func (a *ACLPolicyJobACLFieldIndex) FromObject(obj interface{}) (bool, []byte, e
 	if ns == "" {
 		return false, nil, nil
 	}
+
 	jobID := policy.JobACL.JobID
 	if jobID == "" {
-		return false, nil, fmt.Errorf(
-			"object %#v is not a valid ACLPolicy: Namespace without JobID", obj)
+		return true, []byte(ns + "\x00\x00"), nil
 	}
 
 	val := ns + "\x00" + jobID + "\x00"
@@ -919,19 +919,27 @@ func (a *ACLPolicyJobACLFieldIndex) FromObject(obj interface{}) (bool, []byte, e
 
 // FromArgs is used to build an exact index lookup based on arguments
 func (a *ACLPolicyJobACLFieldIndex) FromArgs(args ...interface{}) ([]byte, error) {
-	if len(args) != 2 {
-		return nil, fmt.Errorf("must provide two arguments")
+	if len(args) < 1 || len(args) > 2 {
+		return nil, fmt.Errorf("must provide one or two arguments")
 	}
 	arg0, ok := args[0].(string)
 	if !ok {
 		return nil, fmt.Errorf("argument must be a string: %#v", args[0])
 	}
+
+	if len(args) == 1 {
+		// Add two null characters to fully terminate a
+		// namespace only entry
+		return []byte(arg0 + "\x00\x00"), nil
+	}
+
 	arg1, ok := args[1].(string)
 	if !ok {
 		return nil, fmt.Errorf("argument must be a string: %#v", args[0])
 	}
 
-	// Add the null character as a terminator
+	// Add the null character as a separator between the
+	// namespace and job id and one for the terminator
 	arg0 += "\x00" + arg1 + "\x00"
 	return []byte(arg0), nil
 }
diff --git a/nomad/state/state_store.go b/nomad/state/state_store.go
index 1f8fcce24..a00656f65 100644
--- a/nomad/state/state_store.go
+++ b/nomad/state/state_store.go
@@ -6127,6 +6127,18 @@ func (s *StateStore) ACLPolicyByJob(ws memdb.WatchSet, ns, jobID string) (memdb.
 	return iter, nil
 }
 
+func (s *StateStore) ACLPolicyByNamespace(ws memdb.WatchSet, ns string) (memdb.ResultIterator, error) {
+	txn := s.db.ReadTxn()
+
+	iter, err := txn.Get("acl_policy", "job", ns)
+	if err != nil {
+		return nil, fmt.Errorf("acl policy lookup failed: %v", err)
+	}
+	ws.Add(iter.WatchCh())
+
+	return iter, nil
+}
+
 // ACLPolicies returns an iterator over all the acl policies
 func (s *StateStore) ACLPolicies(ws memdb.WatchSet) (memdb.ResultIterator, error) {
 	txn := s.db.ReadTxn()
diff --git a/nomad/state/state_store_test.go b/nomad/state/state_store_test.go
index 2b11c8ec7..59e326cc4 100644
--- a/nomad/state/state_store_test.go
+++ b/nomad/state/state_store_test.go
@@ -9142,6 +9142,55 @@ func TestStateStore_UpsertACLPolicy(t *testing.T) {
 	}
 }
 
+func TestStateStore_ACLPolicyByNamespace(t *testing.T) {
+	ci.Parallel(t)
+
+	state := testStateStore(t)
+	policy := mock.ACLPolicy()
+	policy.JobACL = &structs.JobACL{
+		Namespace: "default",
+	}
+	policy1 := mock.ACLPolicy()
+	policy1.JobACL = &structs.JobACL{
+		Namespace: "default",
+		JobID:     "test-ack-job-name",
+	}
+	policy2 := mock.ACLPolicy()
+	policy2.JobACL = &structs.JobACL{
+		Namespace: "default",
+		JobID:     "testing-job",
+	}
+	policy3 := mock.ACLPolicy()
+	policy3.JobACL = &structs.JobACL{
+		Namespace: "testing",
+		JobID:     "test-job",
+	}
+
+	err := state.UpsertACLPolicies(structs.MsgTypeTestSetup, 1000, []*structs.ACLPolicy{policy, policy1, policy2})
+	must.NoError(t, err)
+
+	iter, err := state.ACLPolicyByNamespace(nil, "default")
+	must.NoError(t, err)
+
+	out := iter.Next()
+	must.NotNil(t, out)
+	must.Eq(t, policy, out.(*structs.ACLPolicy))
+
+	count := 0
+	for {
+		if iter.Next() == nil {
+			break
+		}
+
+		count++
+	}
+	must.Eq(t, 0, count)
+
+	iter, err = state.ACLPolicyByNamespace(nil, "testing")
+	must.NoError(t, err)
+	must.Nil(t, iter.Next())
+}
+
 func TestStateStore_DeleteACLPolicy(t *testing.T) {
 	ci.Parallel(t)
 
diff --git a/website/content/docs/concepts/workload-identity.mdx b/website/content/docs/concepts/workload-identity.mdx
index 3caf74cf2..38834ab21 100644
--- a/website/content/docs/concepts/workload-identity.mdx
+++ b/website/content/docs/concepts/workload-identity.mdx
@@ -155,7 +155,7 @@ nomad acl policy apply \
    redis-policy ./policy.hcl
 ```
 
-And you can apply this policy to all groups in the job by omitting both the
+You can apply this policy to all groups in the job by omitting both the
 `-group` and `-task` flag:
 
 ```shell-session
@@ -164,6 +164,14 @@ nomad acl policy apply \
    redis-policy ./policy.hcl
 ```
 
+And you can apply this policy to all jobs in the namespace by omitting the
+`-job`, `-group`, and `-task` flag:
+
+```shell-session
+nomad acl policy apply \
+   -namespace default redis-policy ./policy.hcl
+```
+
 ### Task API
 
 It can be convenient to combine workload identity with Nomad's [Task API]