diff --git a/agent/connect/ca/provider_vault.go b/agent/connect/ca/provider_vault.go
index 8415d07b9a..60627b5314 100644
--- a/agent/connect/ca/provider_vault.go
+++ b/agent/connect/ca/provider_vault.go
@@ -518,7 +518,7 @@ func (v *VaultProvider) ActiveLeafSigningCert() (string, error) {
 // because the endpoint only returns the raw PEM contents of the CA cert
 // and not the typical format of the secrets endpoints.
 func (v *VaultProvider) getCA(namespace, path string) (string, error) {
-	resp, err := v.client.WithNamespace(namespace).Logical().ReadRaw(path + "/ca/pem")
+	resp, err := v.client.WithNamespace(v.getNamespace(namespace)).Logical().ReadRaw(path + "/ca/pem")
 	if resp != nil {
 		defer resp.Body.Close()
 	}
@@ -544,7 +544,7 @@ func (v *VaultProvider) getCA(namespace, path string) (string, error) {
 
 // TODO: refactor to remove duplication with getCA
 func (v *VaultProvider) getCAChain(namespace, path string) (string, error) {
-	resp, err := v.client.WithNamespace(namespace).Logical().ReadRaw(path + "/ca_chain")
+	resp, err := v.client.WithNamespace(v.getNamespace(namespace)).Logical().ReadRaw(path + "/ca_chain")
 	if resp != nil {
 		defer resp.Body.Close()
 	}
@@ -851,27 +851,34 @@ func (v *VaultProvider) Stop() {
 
 // We use raw path here
 func (v *VaultProvider) mountNamespaced(namespace, path string, mountInfo *vaultapi.MountInput) error {
-	return v.client.WithNamespace(namespace).Sys().Mount(path, mountInfo)
+	return v.client.WithNamespace(v.getNamespace(namespace)).Sys().Mount(path, mountInfo)
 }
 
 func (v *VaultProvider) tuneMountNamespaced(namespace, path string, mountConfig *vaultapi.MountConfigInput) error {
-	return v.client.WithNamespace(namespace).Sys().TuneMount(path, *mountConfig)
+	return v.client.WithNamespace(v.getNamespace(namespace)).Sys().TuneMount(path, *mountConfig)
 }
 
 func (v *VaultProvider) unmountNamespaced(namespace, path string) error {
-	return v.client.WithNamespace(namespace).Sys().Unmount(path)
+	return v.client.WithNamespace(v.getNamespace(namespace)).Sys().Unmount(path)
 }
 
 func (v *VaultProvider) readNamespaced(namespace string, resource string) (*vaultapi.Secret, error) {
-	return v.client.WithNamespace(namespace).Logical().Read(resource)
+	return v.client.WithNamespace(v.getNamespace(namespace)).Logical().Read(resource)
 }
 
 func (v *VaultProvider) writeNamespaced(namespace string, resource string, data map[string]interface{}) (*vaultapi.Secret, error) {
-	return v.client.WithNamespace(namespace).Logical().Write(resource, data)
+	return v.client.WithNamespace(v.getNamespace(namespace)).Logical().Write(resource, data)
 }
 
 func (v *VaultProvider) deleteNamespaced(namespace string, resource string) (*vaultapi.Secret, error) {
-	return v.client.WithNamespace(namespace).Logical().Delete(resource)
+	return v.client.WithNamespace(v.getNamespace(namespace)).Logical().Delete(resource)
+}
+
+func (v *VaultProvider) getNamespace(namespace string) string {
+	if namespace != "" {
+		return namespace
+	}
+	return v.baseNamespace
 }
 
 // autotidyIssuers sets Vault's auto-tidy to remove expired issuers
diff --git a/agent/connect/ca/provider_vault_test.go b/agent/connect/ca/provider_vault_test.go
index f7fb8d178a..ece7659d04 100644
--- a/agent/connect/ca/provider_vault_test.go
+++ b/agent/connect/ca/provider_vault_test.go
@@ -1415,6 +1415,85 @@ func TestVaultCAProvider_ConsulManaged(t *testing.T) {
 	})
 }
 
+func TestVaultCAProvider_EnterpriseNamespace(t *testing.T) {
+	SkipIfVaultNotPresent(t, vaultRequirements{Enterprise: true})
+	t.Parallel()
+
+	cases := map[string]struct {
+		namespaces map[string]string
+	}{
+		"no configured namespaces":             {},
+		"only base namespace provided":         {namespaces: map[string]string{"Namespace": "base-ns"}},
+		"only root namespace provided":         {namespaces: map[string]string{"RootPKINamespace": "root-pki-ns"}},
+		"only intermediate namespace provided": {namespaces: map[string]string{"IntermediatePKINamespace": "int-pki-ns"}},
+		"base and root namespace provided": {
+			namespaces: map[string]string{
+				"Namespace":        "base-ns",
+				"RootPKINamespace": "root-pki-ns",
+			},
+		},
+		"base and intermediate namespace provided": {
+			namespaces: map[string]string{
+				"Namespace":                "base-ns",
+				"IntermediatePKINamespace": "int-pki-ns",
+			},
+		},
+		"root and intermediate namespace provided": {
+			namespaces: map[string]string{
+				"RootPKINamespace":         "root-pki-ns",
+				"IntermediatePKINamespace": "int-pki-ns",
+			},
+		},
+		"all namespaces provided": {
+			namespaces: map[string]string{
+				"Namespace":                "base-ns",
+				"RootPKINamespace":         "root-pki-ns",
+				"IntermediatePKINamespace": "int-pki-ns",
+			},
+		},
+	}
+
+	for name, c := range cases {
+		c := c
+		t.Run(name, func(t *testing.T) {
+			t.Parallel()
+
+			testVault := NewTestVaultServer(t)
+			token := "root"
+
+			providerConfig := map[string]any{
+				"RootPKIPath":         "pki-root/",
+				"IntermediatePKIPath": "pki-intermediate/",
+			}
+			for k, v := range c.namespaces {
+				providerConfig[k] = v
+			}
+
+			if len(c.namespaces) > 0 {
+				// If explicit namespaces are provided, try to create the provider before any of the namespaces
+				// have been created. Verify that the provider fails to initialize.
+				provider, err := createVaultProviderE(t, true, testVault.Addr, token, providerConfig)
+				require.Error(t, err)
+				require.NotNil(t, provider)
+			}
+
+			// Create the namespaces
+			client := testVault.Client()
+			client.SetToken(token)
+
+			for _, ns := range c.namespaces {
+				_, err := client.Logical().Write(fmt.Sprintf("/sys/namespaces/%s", ns), map[string]any{})
+				require.NoError(t, err)
+			}
+
+			// Verify that once the namespaces have been created we are able to initialize the provider.
+			provider, err := createVaultProviderE(t, true, testVault.Addr, token, providerConfig)
+			require.NoError(t, err)
+			require.NotNil(t, provider)
+		})
+	}
+}
+
 func getIntermediateCertTTL(t *testing.T, caConf *structs.CAConfiguration) time.Duration {
 	t.Helper()
 
@@ -1436,6 +1515,15 @@ func getIntermediateCertTTL(t *testing.T, caConf *structs.CAConfiguration) time.
 
 func createVaultProvider(t *testing.T, isPrimary bool, addr, token string, rawConf map[string]any) *VaultProvider {
 	t.Helper()
+
+	provider, err := createVaultProviderE(t, isPrimary, addr, token, rawConf)
+	require.NoError(t, err)
+
+	return provider
+}
+
+func createVaultProviderE(t *testing.T, isPrimary bool, addr, token string, rawConf map[string]any) (*VaultProvider, error) {
+	t.Helper()
 	cfg := vaultProviderConfig(t, addr, token, rawConf)
 
 	provider := NewVaultProvider(hclog.New(nil))
@@ -1446,15 +1534,19 @@ func createVaultProvider(t *testing.T, isPrimary bool, addr, token string, rawCo
 	}
 
 	t.Cleanup(provider.Stop)
-	require.NoError(t, provider.Configure(cfg))
+	if err := provider.Configure(cfg); err != nil {
+		return provider, err
+	}
 	if isPrimary {
-		_, err := provider.GenerateCAChain()
-		require.NoError(t, err)
-		_, err = provider.GenerateLeafSigningCert()
-		require.NoError(t, err)
+		if _, err := provider.GenerateCAChain(); err != nil {
+			return provider, err
+		}
+		if _, err := provider.GenerateLeafSigningCert(); err != nil {
+			return provider, err
+		}
 	}
 
-	return provider
+	return provider, nil
 }
 
 func vaultProviderConfig(t *testing.T, addr, token string, rawConf map[string]any) ProviderConfig {
diff --git a/agent/connect/ca/testing.go b/agent/connect/ca/testing.go
index 28d077e34e..7386deea94 100644
--- a/agent/connect/ca/testing.go
+++ b/agent/connect/ca/testing.go
@@ -61,6 +61,10 @@ type CASigningKeyTypes struct {
 	CSRKeyBits     int
 }
 
+type vaultRequirements struct {
+	Enterprise bool
+}
+
 // CASigningKeyTypeCases returns the cross-product of the important supported CA
 // key types for generating table tests for CA signing tests (CrossSignCA and
 // SignIntermediate).
@@ -93,7 +97,7 @@ func TestConsulProvider(t testing.T, d ConsulProviderStateDelegate) *ConsulProvi
 //
 // These tests may be skipped in CI. They are run as part of a separate
 // integration test suite.
-func SkipIfVaultNotPresent(t testing.T) {
+func SkipIfVaultNotPresent(t testing.T, reqs ...vaultRequirements) {
 	// Try to safeguard against tests that will never run in CI.
 	// This substring should match the pattern used by the
 	// test-connect-ca-providers CI job.
@@ -110,6 +114,16 @@ func SkipIfVaultNotPresent(t testing.T) {
 	if err != nil || path == "" {
 		t.Skipf("%q not found on $PATH - download and install to run this test", vaultBinaryName)
 	}
+
+	// Check for any additional Vault requirements.
+	for _, r := range reqs {
+		if r.Enterprise {
+			ver := vaultVersion(t, vaultBinaryName)
+			if !strings.Contains(ver, "+ent") {
+				t.Skipf("%q is not a Vault Enterprise version", ver)
+			}
+		}
+	}
 }
 
 func NewTestVaultServer(t testing.T) *TestVaultServer {
@@ -239,8 +253,8 @@ func requireTrailingNewline(t testing.T, leafPEM string) {
 	if len(leafPEM) == 0 {
 		t.Fatalf("cert is empty")
 	}
-	if '\n' != rune(leafPEM[len(leafPEM)-1]) {
-		t.Fatalf("cert do not end with a new line")
+	if rune(leafPEM[len(leafPEM)-1]) != '\n' {
+		t.Fatalf("cert does not end with a new line")
 	}
 }
 
@@ -367,3 +381,10 @@ func createVaultTokenAndPolicy(t testing.T, client *vaultapi.Client, policyName,
 	require.NoError(t, err)
 	return tok.Auth.ClientToken
 }
+
+func vaultVersion(t testing.T, vaultBinaryName string) string {
+	cmd := exec.Command(vaultBinaryName, []string{"version"}...)
+	output, err := cmd.Output()
+	require.NoError(t, err)
+	return string(output[:len(output)-1])
+}