diff --git a/client/allocrunner/alloc_runner_hooks.go b/client/allocrunner/alloc_runner_hooks.go
index d0ed29c43..9769a6cb0 100644
--- a/client/allocrunner/alloc_runner_hooks.go
+++ b/client/allocrunner/alloc_runner_hooks.go
@@ -117,6 +117,7 @@ func (ar *allocRunner) initRunnerHooks(config *clientconfig.Config) error {
 	// Create the alloc directory hook. This is run first to ensure the
 	// directory path exists for other hooks.
 	alloc := ar.Alloc()
+
 	ar.runnerHooks = []interfaces.RunnerHook{
 		newIdentityHook(hookLogger, ar.widmgr),
 		newAllocDirHook(hookLogger, ar.allocDir),
@@ -145,8 +146,10 @@ func (ar *allocRunner) initRunnerHooks(config *clientconfig.Config) error {
 			logger:            hookLogger,
 			shutdownDelayCtx:  ar.shutdownDelayCtx,
 		}),
-		newConsulGRPCSocketHook(hookLogger, alloc, ar.allocDir, config.ConsulConfig, config.Node.Attributes),
-		newConsulHTTPSocketHook(hookLogger, alloc, ar.allocDir, config.ConsulConfig),
+		newConsulGRPCSocketHook(hookLogger, alloc, ar.allocDir,
+			config.GetConsulConfigs(ar.logger), config.Node.Attributes),
+		newConsulHTTPSocketHook(hookLogger, alloc, ar.allocDir,
+			config.GetConsulConfigs(ar.logger)),
 		newCSIHook(alloc, hookLogger, ar.csiManager, ar.rpcClient, ar, ar.hookResources, ar.clientConfig.Node.SecretID),
 		newChecksHook(hookLogger, alloc, ar.checkStore, ar, builtTaskEnv),
 	}
diff --git a/client/allocrunner/consul_grpc_sock_hook.go b/client/allocrunner/consul_grpc_sock_hook.go
index 7ff085141..2ee814bf6 100644
--- a/client/allocrunner/consul_grpc_sock_hook.go
+++ b/client/allocrunner/consul_grpc_sock_hook.go
@@ -16,6 +16,8 @@ import (
 	"time"
 
 	"github.com/hashicorp/go-hclog"
+	multierror "github.com/hashicorp/go-multierror"
+	"github.com/hashicorp/go-set/v2"
 	"github.com/hashicorp/nomad/client/allocdir"
 	"github.com/hashicorp/nomad/client/allocrunner/interfaces"
 	"github.com/hashicorp/nomad/nomad/structs"
@@ -48,26 +50,46 @@ type consulGRPCSocketHook struct {
 
 	// mu synchronizes proxy and alloc which may be mutated and read concurrently
 	// via Prerun, Update, Postrun.
-	mu    sync.Mutex
-	alloc *structs.Allocation
-	proxy *grpcSocketProxy
+	mu      sync.Mutex
+	alloc   *structs.Allocation
+	proxies map[string]*grpcSocketProxy
 }
 
 func newConsulGRPCSocketHook(
 	logger hclog.Logger, alloc *structs.Allocation, allocDir *allocdir.AllocDir,
-	config *config.ConsulConfig, nodeAttrs map[string]string) *consulGRPCSocketHook {
+	configs map[string]*config.ConsulConfig, nodeAttrs map[string]string) *consulGRPCSocketHook {
 
-	// Attempt to find the gRPC port via the node attributes, otherwise use the
-	// default fallback.
-	consulGRPCPort, ok := nodeAttrs["consul.grpc"]
-	if !ok {
-		consulGRPCPort = consulGRPCFallbackPort
+	// Get the deduplicated set of Consul clusters that are needed by this
+	// alloc. For Nomad CE, this will always be just the default cluster.
+	clusterNames := set.New[string](1)
+	tg := alloc.Job.LookupTaskGroup(alloc.TaskGroup)
+	for _, s := range tg.Services {
+		clusterNames.Insert(s.GetConsulClusterName(tg))
 	}
+	proxies := map[string]*grpcSocketProxy{}
+
+	clusterNames.ForEach(func(clusterName string) bool {
+
+		// Attempt to find the gRPC port via the node attributes, otherwise use
+		// the default fallback.
+		attrName := "consul.grpc"
+		if clusterName != structs.ConsulDefaultCluster {
+			attrName = "consul." + clusterName + ".grpc"
+		}
+		consulGRPCPort, ok := nodeAttrs[attrName]
+		if !ok {
+			consulGRPCPort = consulGRPCFallbackPort
+		}
+
+		proxies[clusterName] = newGRPCSocketProxy(logger, allocDir,
+			configs[clusterName], consulGRPCPort)
+		return true
+	})
 
 	return &consulGRPCSocketHook{
-		alloc:  alloc,
-		proxy:  newGRPCSocketProxy(logger, allocDir, config, consulGRPCPort),
-		logger: logger.Named(consulGRPCSockHookName),
+		alloc:   alloc,
+		proxies: proxies,
+		logger:  logger.Named(consulGRPCSockHookName),
 	}
 }
 
@@ -102,7 +124,13 @@ func (h *consulGRPCSocketHook) Prerun() error {
 		return nil
 	}
 
-	return h.proxy.run(h.alloc)
+	var mErr *multierror.Error
+	for _, proxy := range h.proxies {
+		if err := proxy.run(h.alloc); err != nil {
+			mErr = multierror.Append(mErr, err)
+		}
+	}
+	return mErr.ErrorOrNil()
 }
 
 // Update creates a gRPC socket file and proxy if there are any Connect
@@ -116,19 +144,31 @@ func (h *consulGRPCSocketHook) Update(req *interfaces.RunnerUpdateRequest) error
 	if !h.shouldRun() {
 		return nil
 	}
+	if len(h.proxies) == 0 {
+		return fmt.Errorf("cannot update alloc to Connect in-place")
+	}
 
-	return h.proxy.run(h.alloc)
+	var mErr *multierror.Error
+	for _, proxy := range h.proxies {
+		if err := proxy.run(h.alloc); err != nil {
+			mErr = multierror.Append(mErr, err)
+		}
+	}
+	return mErr.ErrorOrNil()
 }
 
 func (h *consulGRPCSocketHook) Postrun() error {
 	h.mu.Lock()
 	defer h.mu.Unlock()
 
-	if err := h.proxy.stop(); err != nil {
-		// Only log failures to stop proxies. Worst case scenario is a
-		// small goroutine leak.
-		h.logger.Debug("error stopping Consul proxy", "error", err)
+	for _, proxy := range h.proxies {
+		if err := proxy.stop(); err != nil {
+			// Only log failures to stop proxies. Worst case scenario is a small
+			// goroutine leak.
+			h.logger.Warn("error stopping Consul proxy", "error", err)
+		}
 	}
+
 	return nil
 }
 
@@ -186,7 +226,8 @@ func (p *grpcSocketProxy) run(alloc *structs.Allocation) error {
 
 	// make sure either grpc or http consul address has been configured
 	if p.config.GRPCAddr == "" && p.config.Addr == "" {
-		return errors.New("consul address must be set on nomad client")
+		return fmt.Errorf("consul address for cluster %q must be set on nomad client",
+			p.config.Name)
 	}
 
 	destAddr := p.config.GRPCAddr
@@ -195,13 +236,17 @@ func (p *grpcSocketProxy) run(alloc *structs.Allocation) error {
 		// default of 8502.
 		host, _, err := net.SplitHostPort(p.config.Addr)
 		if err != nil {
-			return fmt.Errorf("error parsing Consul address %q: %v",
-				p.config.Addr, err)
+			return fmt.Errorf("error parsing Consul address %q: %v", p.config.Addr, err)
 		}
 		destAddr = net.JoinHostPort(host, p.consulGRPCFallbackPort)
 	}
 
-	hostGRPCSocketPath := filepath.Join(p.allocDir.AllocDir, allocdir.AllocGRPCSocket)
+	socketFile := allocdir.AllocGRPCSocket
+	if p.config.Name != structs.ConsulDefaultCluster && p.config.Name != "" {
+		socketFile = filepath.Join(allocdir.SharedAllocName, allocdir.TmpDirName,
+			"consul_"+p.config.Name+"_grpc.sock")
+	}
+	hostGRPCSocketPath := filepath.Join(p.allocDir.AllocDir, socketFile)
 
 	// if the socket already exists we'll try to remove it, but if not then any
 	// other errors will bubble up to the caller here or when we try to listen
diff --git a/client/allocrunner/consul_grpc_sock_hook_test.go b/client/allocrunner/consul_grpc_sock_hook_test.go
index b08d4575c..8ed87f85e 100644
--- a/client/allocrunner/consul_grpc_sock_hook_test.go
+++ b/client/allocrunner/consul_grpc_sock_hook_test.go
@@ -17,7 +17,9 @@ import (
 	"github.com/hashicorp/nomad/client/allocrunner/interfaces"
 	"github.com/hashicorp/nomad/helper/testlog"
 	"github.com/hashicorp/nomad/nomad/mock"
+	"github.com/hashicorp/nomad/nomad/structs"
 	"github.com/hashicorp/nomad/nomad/structs/config"
+	"github.com/shoenig/test/must"
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
 )
@@ -33,9 +35,11 @@ func TestConsulGRPCSocketHook_PrerunPostrun_Ok(t *testing.T) {
 	fakeConsul, err := net.Listen("tcp", "127.0.0.1:0")
 	require.NoError(t, err)
 	defer fakeConsul.Close()
-	consulConfig := &config.ConsulConfig{
-		GRPCAddr: fakeConsul.Addr().String(),
-	}
+
+	consulConfigs := map[string]*config.ConsulConfig{
+		structs.ConsulDefaultCluster: {
+			GRPCAddr: fakeConsul.Addr().String(),
+		}}
 
 	alloc := mock.ConnectAlloc()
 
@@ -45,7 +49,7 @@ func TestConsulGRPCSocketHook_PrerunPostrun_Ok(t *testing.T) {
 	defer cleanup()
 
 	// Start the unix socket proxy
-	h := newConsulGRPCSocketHook(logger, alloc, allocDir, consulConfig, map[string]string{})
+	h := newConsulGRPCSocketHook(logger, alloc, allocDir, consulConfigs, map[string]string{})
 	require.NoError(t, h.Prerun())
 
 	gRPCSock := filepath.Join(allocDir.AllocDir, allocdir.AllocGRPCSocket)
@@ -108,7 +112,8 @@ func TestConsulGRPCSocketHook_Prerun_Error(t *testing.T) {
 	logger := testlog.HCLogger(t)
 
 	// A config without an Addr or GRPCAddr is invalid.
-	consulConfig := &config.ConsulConfig{}
+	consulConfigs := map[string]*config.ConsulConfig{
+		structs.ConsulDefaultCluster: {}}
 
 	alloc := mock.Alloc()
 	connectAlloc := mock.ConnectAlloc()
@@ -119,36 +124,36 @@ func TestConsulGRPCSocketHook_Prerun_Error(t *testing.T) {
 	{
 		// An alloc without a Connect proxy sidecar should not return
 		// an error.
-		h := newConsulGRPCSocketHook(logger, alloc, allocDir, consulConfig, map[string]string{})
-		require.NoError(t, h.Prerun())
+		h := newConsulGRPCSocketHook(logger, alloc, allocDir, consulConfigs, map[string]string{})
+		must.NoError(t, h.Prerun())
 
 		// Postrun should be a noop
-		require.NoError(t, h.Postrun())
+		must.NoError(t, h.Postrun())
 	}
 
 	{
 		// An alloc *with* a Connect proxy sidecar *should* return an error
 		// when Consul is not configured.
-		h := newConsulGRPCSocketHook(logger, connectAlloc, allocDir, consulConfig, map[string]string{})
-		require.EqualError(t, h.Prerun(), "consul address must be set on nomad client")
+		h := newConsulGRPCSocketHook(logger, connectAlloc, allocDir, consulConfigs, map[string]string{})
+		must.ErrorContains(t, h.Prerun(), `consul address for cluster "" must be set on nomad client`)
 
 		// Postrun should be a noop
-		require.NoError(t, h.Postrun())
+		must.NoError(t, h.Postrun())
 	}
 
 	{
 		// Updating an alloc without a sidecar to have a sidecar should
 		// error when the sidecar is added.
-		h := newConsulGRPCSocketHook(logger, alloc, allocDir, consulConfig, map[string]string{})
-		require.NoError(t, h.Prerun())
+		h := newConsulGRPCSocketHook(logger, alloc, allocDir, consulConfigs, map[string]string{})
+		must.NoError(t, h.Prerun())
 
 		req := &interfaces.RunnerUpdateRequest{
 			Alloc: connectAlloc,
 		}
-		require.EqualError(t, h.Update(req), "consul address must be set on nomad client")
+		must.EqError(t, h.Update(req), "cannot update alloc to Connect in-place")
 
 		// Postrun should be a noop
-		require.NoError(t, h.Postrun())
+		must.NoError(t, h.Postrun())
 	}
 }
 
diff --git a/client/allocrunner/consul_http_sock_hook.go b/client/allocrunner/consul_http_sock_hook.go
index 7c725c8d0..eaf535984 100644
--- a/client/allocrunner/consul_http_sock_hook.go
+++ b/client/allocrunner/consul_http_sock_hook.go
@@ -14,6 +14,8 @@ import (
 	"time"
 
 	"github.com/hashicorp/go-hclog"
+	multierror "github.com/hashicorp/go-multierror"
+	"github.com/hashicorp/go-set/v2"
 	"github.com/hashicorp/nomad/client/allocdir"
 	"github.com/hashicorp/nomad/client/allocrunner/interfaces"
 	"github.com/hashicorp/nomad/nomad/structs"
@@ -36,16 +38,31 @@ type consulHTTPSockHook struct {
 
 	// lock synchronizes proxy and alloc which may be mutated and read concurrently
 	// via Prerun, Update, and Postrun.
-	lock  sync.Mutex
-	alloc *structs.Allocation
-	proxy *httpSocketProxy
+	lock    sync.Mutex
+	alloc   *structs.Allocation
+	proxies map[string]*httpSocketProxy
 }
 
-func newConsulHTTPSocketHook(logger hclog.Logger, alloc *structs.Allocation, allocDir *allocdir.AllocDir, config *config.ConsulConfig) *consulHTTPSockHook {
+func newConsulHTTPSocketHook(logger hclog.Logger, alloc *structs.Allocation, allocDir *allocdir.AllocDir, configs map[string]*config.ConsulConfig) *consulHTTPSockHook {
+
+	// Get the deduplicated set of Consul clusters that are needed by this
+	// alloc. For Nomad CE, this will always be just the default cluster.
+	clusterNames := set.New[string](1)
+	tg := alloc.Job.LookupTaskGroup(alloc.TaskGroup)
+	for _, s := range tg.Services {
+		clusterNames.Insert(s.GetConsulClusterName(tg))
+	}
+	proxies := map[string]*httpSocketProxy{}
+
+	clusterNames.ForEach(func(clusterName string) bool {
+		proxies[clusterName] = newHTTPSocketProxy(logger, allocDir, configs[clusterName])
+		return true
+	})
+
 	return &consulHTTPSockHook{
-		alloc:  alloc,
-		proxy:  newHTTPSocketProxy(logger, allocDir, config),
-		logger: logger.Named(consulHTTPSocketHookName),
+		alloc:   alloc,
+		proxies: proxies,
+		logger:  logger.Named(consulHTTPSocketHookName),
 	}
 }
 
@@ -81,7 +98,13 @@ func (h *consulHTTPSockHook) Prerun() error {
 		return nil
 	}
 
-	return h.proxy.run(h.alloc)
+	var mErr *multierror.Error
+	for _, proxy := range h.proxies {
+		if err := proxy.run(h.alloc); err != nil {
+			mErr = multierror.Append(mErr, err)
+		}
+	}
+	return mErr.ErrorOrNil()
 }
 
 func (h *consulHTTPSockHook) Update(req *interfaces.RunnerUpdateRequest) error {
@@ -93,17 +116,29 @@ func (h *consulHTTPSockHook) Update(req *interfaces.RunnerUpdateRequest) error {
 	if !h.shouldRun() {
 		return nil
 	}
+	if len(h.proxies) == 0 {
+		return fmt.Errorf("cannot update alloc to Connect in-place")
+	}
 
-	return h.proxy.run(h.alloc)
+	var mErr *multierror.Error
+	for _, proxy := range h.proxies {
+		if err := proxy.run(h.alloc); err != nil {
+			mErr = multierror.Append(mErr, err)
+		}
+	}
+	return mErr.ErrorOrNil()
 }
 
 func (h *consulHTTPSockHook) Postrun() error {
 	h.lock.Lock()
 	defer h.lock.Unlock()
 
-	if err := h.proxy.stop(); err != nil {
-		// Only log a failure to stop, worst case is the proxy leaks a goroutine.
-		h.logger.Warn("error stopping Consul HTTP proxy", "error", err)
+	for _, proxy := range h.proxies {
+		if err := proxy.stop(); err != nil {
+			// Only log failures to stop proxies. Worst case scenario is a small
+			// goroutine leak.
+			h.logger.Warn("error stopping Consul HTTP proxy", "error", err)
+		}
 	}
 
 	return nil
@@ -158,7 +193,12 @@ func (p *httpSocketProxy) run(alloc *structs.Allocation) error {
 		return errors.New("consul address must be set on nomad client")
 	}
 
-	hostHTTPSockPath := filepath.Join(p.allocDir.AllocDir, allocdir.AllocHTTPSocket)
+	socketFile := allocdir.AllocHTTPSocket
+	if p.config.Name != structs.ConsulDefaultCluster && p.config.Name != "" {
+		socketFile = filepath.Join(allocdir.SharedAllocName, allocdir.TmpDirName,
+			"consul_"+p.config.Name+"_http.sock")
+	}
+	hostHTTPSockPath := filepath.Join(p.allocDir.AllocDir, socketFile)
 	if err := maybeRemoveOldSocket(hostHTTPSockPath); err != nil {
 		return err
 	}
diff --git a/client/allocrunner/consul_http_sock_hook_test.go b/client/allocrunner/consul_http_sock_hook_test.go
index 022da2018..a6a31ec2c 100644
--- a/client/allocrunner/consul_http_sock_hook_test.go
+++ b/client/allocrunner/consul_http_sock_hook_test.go
@@ -13,7 +13,9 @@ import (
 	"github.com/hashicorp/nomad/client/allocdir"
 	"github.com/hashicorp/nomad/helper/testlog"
 	"github.com/hashicorp/nomad/nomad/mock"
+	"github.com/hashicorp/nomad/nomad/structs"
 	"github.com/hashicorp/nomad/nomad/structs/config"
+	"github.com/shoenig/test/must"
 	"github.com/stretchr/testify/require"
 )
 
@@ -24,8 +26,8 @@ func TestConsulSocketHook_PrerunPostrun_Ok(t *testing.T) {
 	require.NoError(t, err)
 	defer fakeConsul.Close()
 
-	consulConfig := &config.ConsulConfig{
-		Addr: fakeConsul.Addr().String(),
+	consulConfigs := map[string]*config.ConsulConfig{
+		structs.ConsulDefaultCluster: {Addr: fakeConsul.Addr().String()},
 	}
 
 	alloc := mock.ConnectNativeAlloc("bridge")
@@ -36,7 +38,7 @@ func TestConsulSocketHook_PrerunPostrun_Ok(t *testing.T) {
 	defer cleanupDir()
 
 	// start unix socket proxy
-	h := newConsulHTTPSocketHook(logger, alloc, allocDir, consulConfig)
+	h := newConsulHTTPSocketHook(logger, alloc, allocDir, consulConfigs)
 	require.NoError(t, h.Prerun())
 
 	httpSocket := filepath.Join(allocDir.AllocDir, allocdir.AllocHTTPSocket)
@@ -97,7 +99,9 @@ func TestConsulHTTPSocketHook_Prerun_Error(t *testing.T) {
 
 	logger := testlog.HCLogger(t)
 
-	consulConfig := new(config.ConsulConfig)
+	consulConfigs := map[string]*config.ConsulConfig{
+		structs.ConsulDefaultCluster: new(config.ConsulConfig),
+	}
 
 	alloc := mock.Alloc()
 	connectNativeAlloc := mock.ConnectNativeAlloc("bridge")
@@ -107,20 +111,20 @@ func TestConsulHTTPSocketHook_Prerun_Error(t *testing.T) {
 
 	{
 		// an alloc without a connect native task should not return an error
-		h := newConsulHTTPSocketHook(logger, alloc, allocDir, consulConfig)
-		require.NoError(t, h.Prerun())
+		h := newConsulHTTPSocketHook(logger, alloc, allocDir, consulConfigs)
+		must.NoError(t, h.Prerun())
 
 		// postrun should be a noop
-		require.NoError(t, h.Postrun())
+		must.NoError(t, h.Postrun())
 	}
 
 	{
 		// an alloc with a native task should return an error when consul is not
 		// configured
-		h := newConsulHTTPSocketHook(logger, connectNativeAlloc, allocDir, consulConfig)
-		require.EqualError(t, h.Prerun(), "consul address must be set on nomad client")
+		h := newConsulHTTPSocketHook(logger, connectNativeAlloc, allocDir, consulConfigs)
+		must.ErrorContains(t, h.Prerun(), "consul address must be set on nomad client")
 
 		// Postrun should be a noop
-		require.NoError(t, h.Postrun())
+		must.NoError(t, h.Postrun())
 	}
 }
diff --git a/client/allocrunner/taskrunner/envoy_version_hook.go b/client/allocrunner/taskrunner/envoy_version_hook.go
index b34848b34..6c342614b 100644
--- a/client/allocrunner/taskrunner/envoy_version_hook.go
+++ b/client/allocrunner/taskrunner/envoy_version_hook.go
@@ -82,7 +82,7 @@ func (h *envoyVersionHook) Prestart(_ context.Context, request *ifs.TaskPrestart
 	// We either need to acquire Consul's preferred Envoy version or fallback
 	// to the legacy default. Query Consul and use the (possibly empty) result.
 	//
-	// TODO: how do we select the right cluster here if we have multiple
+	// TODO(tgross): how do we select the right cluster here if we have multiple
 	// services which could have their own cluster field value?
 	proxies, err := h.proxiesClientFunc(structs.ConsulDefaultCluster).Proxies()
 	if err != nil {
diff --git a/client/allocrunner/taskrunner/sids_hook_test.go b/client/allocrunner/taskrunner/sids_hook_test.go
index e617a313d..82890f5da 100644
--- a/client/allocrunner/taskrunner/sids_hook_test.go
+++ b/client/allocrunner/taskrunner/sids_hook_test.go
@@ -284,7 +284,7 @@ func TestTaskRunner_DeriveSIToken_UnWritableTokenFile(t *testing.T) {
 
 	// set a consul token for the nomad client, which is what triggers the
 	// SIDS hook to be applied
-	trConfig.ClientConfig.ConsulConfig.Token = uuid.Generate()
+	trConfig.ClientConfig.GetDefaultConsul().Token = uuid.Generate()
 
 	// derive token works just fine
 	deriveFn := func(*structs.Allocation, []string) (map[string]string, error) {
diff --git a/client/allocrunner/taskrunner/task_runner_getters.go b/client/allocrunner/taskrunner/task_runner_getters.go
index 94879402d..925d1cc5b 100644
--- a/client/allocrunner/taskrunner/task_runner_getters.go
+++ b/client/allocrunner/taskrunner/task_runner_getters.go
@@ -72,7 +72,7 @@ func (tr *TaskRunner) setVaultToken(token string) {
 	// Update the task's environment
 	taskNamespace := tr.task.Vault.Namespace
 
-	ns := tr.clientConfig.VaultConfig.Namespace
+	ns := tr.clientConfig.GetVaultConfigs(tr.logger)[tr.task.GetVaultClusterName()].Namespace
 	if taskNamespace != "" {
 		ns = taskNamespace
 	}
diff --git a/client/allocrunner/taskrunner/task_runner_hooks.go b/client/allocrunner/taskrunner/task_runner_hooks.go
index 6261dc9b5..806f429cf 100644
--- a/client/allocrunner/taskrunner/task_runner_hooks.go
+++ b/client/allocrunner/taskrunner/task_runner_hooks.go
@@ -142,9 +142,11 @@ func (tr *TaskRunner) initHooks() {
 	// If this is a Connect sidecar proxy (or a Connect Native) service,
 	// add the sidsHook for requesting a Service Identity token (if ACLs).
 	if task.UsesConnect() {
+		tg := tr.Alloc().Job.LookupTaskGroup(tr.Alloc().TaskGroup)
+
 		// Enable the Service Identity hook only if the Nomad client is configured
 		// with a consul token, indicating that Consul ACLs are enabled
-		if tr.clientConfig.ConsulConfig.Token != "" {
+		if tr.clientConfig.GetConsulConfigs(tr.logger)[task.GetConsulClusterName(tg)].Token != "" {
 			tr.runnerHooks = append(tr.runnerHooks, newSIDSHook(sidsHookConfig{
 				alloc:              tr.Alloc(),
 				task:               tr.Task(),
@@ -158,11 +160,15 @@ func (tr *TaskRunner) initHooks() {
 		if task.UsesConnectSidecar() {
 			tr.runnerHooks = append(tr.runnerHooks,
 				newEnvoyVersionHook(newEnvoyVersionHookConfig(alloc, tr.consulProxiesClientFunc, hookLogger)),
-				newEnvoyBootstrapHook(newEnvoyBootstrapHookConfig(alloc, tr.clientConfig.ConsulConfig, consulNamespace, hookLogger)),
+				newEnvoyBootstrapHook(newEnvoyBootstrapHookConfig(alloc,
+					tr.clientConfig.ConsulConfigs[task.GetConsulClusterName(tg)],
+					consulNamespace,
+					hookLogger)),
 			)
 		} else if task.Kind.IsConnectNative() {
 			tr.runnerHooks = append(tr.runnerHooks, newConnectNativeHook(
-				newConnectNativeHookConfig(alloc, tr.clientConfig.ConsulConfig, hookLogger),
+				newConnectNativeHookConfig(alloc,
+					tr.clientConfig.ConsulConfigs[task.GetConsulClusterName(tg)], hookLogger),
 			))
 		}
 	}
diff --git a/client/allocrunner/taskrunner/task_runner_test.go b/client/allocrunner/taskrunner/task_runner_test.go
index 290bde161..2bd0741ba 100644
--- a/client/allocrunner/taskrunner/task_runner_test.go
+++ b/client/allocrunner/taskrunner/task_runner_test.go
@@ -122,7 +122,7 @@ func testTaskRunnerConfig(t *testing.T, alloc *structs.Allocation, taskName stri
 	db := cstate.NewMemDB(logger)
 
 	if thisTask.Vault != nil {
-		clientConf.VaultConfigs[structs.VaultDefaultCluster].Enabled = pointer.Of(true)
+		clientConf.GetDefaultVault().Enabled = pointer.Of(true)
 	}
 
 	var vaultFunc vaultclient.VaultClientFunc
@@ -1433,7 +1433,7 @@ func TestTaskRunner_BlockForSIDSToken(t *testing.T) {
 
 	// set a consul token on the Nomad client's consul config, because that is
 	// what gates the action of requesting SI token(s)
-	trConfig.ClientConfig.ConsulConfig.Token = uuid.Generate()
+	trConfig.ClientConfig.GetDefaultConsul().Token = uuid.Generate()
 
 	// control when we get a Consul SI token
 	token := uuid.Generate()
@@ -1497,7 +1497,7 @@ func TestTaskRunner_DeriveSIToken_Retry(t *testing.T) {
 
 	// set a consul token on the Nomad client's consul config, because that is
 	// what gates the action of requesting SI token(s)
-	trConfig.ClientConfig.ConsulConfig.Token = uuid.Generate()
+	trConfig.ClientConfig.GetDefaultConsul().Token = uuid.Generate()
 
 	// control when we get a Consul SI token (recoverable failure on first call)
 	token := uuid.Generate()
@@ -1557,7 +1557,7 @@ func TestTaskRunner_DeriveSIToken_Unrecoverable(t *testing.T) {
 
 	// set a consul token on the Nomad client's consul config, because that is
 	// what gates the action of requesting SI token(s)
-	trConfig.ClientConfig.ConsulConfig.Token = uuid.Generate()
+	trConfig.ClientConfig.GetDefaultConsul().Token = uuid.Generate()
 
 	// SI token derivation suffers a non-retryable error
 	siClient := trConfig.ConsulSI.(*consulapi.MockServiceIdentitiesClient)
diff --git a/client/allocrunner/taskrunner/template/template.go b/client/allocrunner/taskrunner/template/template.go
index c2a6543c0..a5e038fc6 100644
--- a/client/allocrunner/taskrunner/template/template.go
+++ b/client/allocrunner/taskrunner/template/template.go
@@ -100,6 +100,10 @@ type TaskTemplateManagerConfig struct {
 	// workload identity
 	ConsulToken string
 
+	// ConsulConfig is the Consul configuration to use for this template. It may
+	// be nil if Nomad has no Consul cofiguration
+	ConsulConfig *structsc.ConsulConfig
+
 	// VaultToken is the Vault token for the task.
 	VaultToken string
 
@@ -819,8 +823,8 @@ func newRunnerConfig(config *TaskTemplateManagerConfig,
 	}
 
 	// Set up the Consul config
-	if cc.ConsulConfig != nil {
-		conf.Consul.Address = &cc.ConsulConfig.Addr
+	if config.ConsulConfig != nil {
+		conf.Consul.Address = &config.ConsulConfig.Addr
 
 		// if we're using WI, use the token from consul_hook
 		// NOTE: from Nomad 1.9 on, WI will be the only supported way of
@@ -828,28 +832,28 @@ func newRunnerConfig(config *TaskTemplateManagerConfig,
 		if config.ConsulToken != "" {
 			conf.Consul.Token = &config.ConsulToken
 		} else {
-			conf.Consul.Token = &cc.ConsulConfig.Token
+			conf.Consul.Token = &config.ConsulConfig.Token
 		}
 
 		// Get the Consul namespace from agent config. This is the lower level
 		// of precedence (beyond default).
-		if cc.ConsulConfig.Namespace != "" {
-			conf.Consul.Namespace = &cc.ConsulConfig.Namespace
+		if config.ConsulConfig.Namespace != "" {
+			conf.Consul.Namespace = &config.ConsulConfig.Namespace
 		}
 
-		if cc.ConsulConfig.EnableSSL != nil && *cc.ConsulConfig.EnableSSL {
-			verify := cc.ConsulConfig.VerifySSL != nil && *cc.ConsulConfig.VerifySSL
+		if config.ConsulConfig.EnableSSL != nil && *config.ConsulConfig.EnableSSL {
+			verify := config.ConsulConfig.VerifySSL != nil && *config.ConsulConfig.VerifySSL
 			conf.Consul.SSL = &ctconf.SSLConfig{
 				Enabled: pointer.Of(true),
 				Verify:  &verify,
-				Cert:    &cc.ConsulConfig.CertFile,
-				Key:     &cc.ConsulConfig.KeyFile,
-				CaCert:  &cc.ConsulConfig.CAFile,
+				Cert:    &config.ConsulConfig.CertFile,
+				Key:     &config.ConsulConfig.KeyFile,
+				CaCert:  &config.ConsulConfig.CAFile,
 			}
 		}
 
-		if cc.ConsulConfig.Auth != "" {
-			parts := strings.SplitN(cc.ConsulConfig.Auth, ":", 2)
+		if config.ConsulConfig.Auth != "" {
+			parts := strings.SplitN(config.ConsulConfig.Auth, ":", 2)
 			if len(parts) != 2 {
 				return nil, fmt.Errorf("Failed to parse Consul Auth config")
 			}
diff --git a/client/allocrunner/taskrunner/template/template_test.go b/client/allocrunner/taskrunner/template/template_test.go
index dcb1f378b..d617898e4 100644
--- a/client/allocrunner/taskrunner/template/template_test.go
+++ b/client/allocrunner/taskrunner/template/template_test.go
@@ -114,9 +114,10 @@ func newTestHarness(t *testing.T, templates []*structs.Template, consul, vault b
 		if err != nil {
 			t.Fatalf("error starting test Consul server: %v", err)
 		}
-		harness.config.ConsulConfig = &sconfig.ConsulConfig{
-			Addr: harness.consul.HTTPAddr,
-		}
+		harness.config.ConsulConfigs = map[string]*sconfig.ConsulConfig{
+			structs.ConsulDefaultCluster: {
+				Addr: harness.consul.HTTPAddr,
+			}}
 	}
 
 	if vault {
@@ -124,7 +125,6 @@ func newTestHarness(t *testing.T, templates []*structs.Template, consul, vault b
 		harness.config.VaultConfigs = map[string]*sconfig.VaultConfig{
 			structs.VaultDefaultCluster: harness.vault.Config,
 		}
-		harness.config.VaultConfig = harness.config.VaultConfigs[structs.VaultDefaultCluster]
 		harness.vaultToken = harness.vault.RootToken
 	}
 
@@ -145,8 +145,9 @@ func (h *testHarness) startWithErr() error {
 		Events:               h.mockHooks,
 		Templates:            h.templates,
 		ClientConfig:         h.config,
+		ConsulConfig:         h.config.GetDefaultConsul(),
 		VaultToken:           h.vaultToken,
-		VaultConfig:          h.config.VaultConfigs[structs.VaultDefaultCluster],
+		VaultConfig:          h.config.GetDefaultVault(),
 		TaskDir:              h.taskDir,
 		EnvBuilder:           h.envBuilder,
 		MaxTemplateEventRate: h.emitRate,
@@ -1716,20 +1717,19 @@ func TestTaskTemplateManager_Config_ServerName(t *testing.T) {
 			TLSServerName: "notlocalhost",
 		},
 	}
-	c.VaultConfig = c.VaultConfigs[structs.VaultDefaultCluster]
 
 	config := &TaskTemplateManagerConfig{
 		ClientConfig: c,
 		VaultToken:   "token",
-		VaultConfig:  c.VaultConfigs[structs.VaultDefaultCluster],
+		VaultConfig:  c.GetDefaultVault(),
 	}
 	ctconf, err := newRunnerConfig(config, nil)
 	if err != nil {
 		t.Fatalf("unexpected error: %v", err)
 	}
 
-	if *ctconf.Vault.SSL.ServerName != c.VaultConfig.TLSServerName {
-		t.Fatalf("expected %q but found %q", c.VaultConfig.TLSServerName, *ctconf.Vault.SSL.ServerName)
+	if *ctconf.Vault.SSL.ServerName != c.GetDefaultVault().TLSServerName {
+		t.Fatalf("expected %q but found %q", c.GetDefaultVault().TLSServerName, *ctconf.Vault.SSL.ServerName)
 	}
 }
 
@@ -1750,13 +1750,12 @@ func TestTaskTemplateManager_Config_VaultNamespace(t *testing.T) {
 			Namespace:     testNS,
 		},
 	}
-	c.VaultConfig = c.VaultConfigs[structs.VaultDefaultCluster]
 
 	alloc := mock.Alloc()
 	config := &TaskTemplateManagerConfig{
 		ClientConfig: c,
 		VaultToken:   "token",
-		VaultConfig:  c.VaultConfigs[structs.VaultDefaultCluster],
+		VaultConfig:  c.GetDefaultVault(),
 		EnvBuilder:   taskenv.NewBuilder(c.Node, alloc, alloc.Job.TaskGroups[0].Tasks[0], c.Region),
 	}
 
@@ -1785,7 +1784,6 @@ func TestTaskTemplateManager_Config_VaultNamespace_TaskOverride(t *testing.T) {
 			Namespace:     testNS,
 		},
 	}
-	c.VaultConfig = c.VaultConfigs[structs.VaultDefaultCluster]
 
 	alloc := mock.Alloc()
 	overriddenNS := "new-namespace"
@@ -1794,7 +1792,7 @@ func TestTaskTemplateManager_Config_VaultNamespace_TaskOverride(t *testing.T) {
 	config := &TaskTemplateManagerConfig{
 		ClientConfig:   c,
 		VaultToken:     "token",
-		VaultConfig:    c.VaultConfigs[structs.VaultDefaultCluster],
+		VaultConfig:    c.GetDefaultVault(),
 		VaultNamespace: overriddenNS,
 		EnvBuilder:     taskenv.NewBuilder(c.Node, alloc, alloc.Job.TaskGroups[0].Tasks[0], c.Region),
 	}
@@ -2173,11 +2171,10 @@ func TestTaskTemplateManager_ClientTemplateConfig_Set(t *testing.T) {
 			Namespace: testNS,
 		},
 	}
-	clientConfig.VaultConfig = clientConfig.VaultConfigs[structs.VaultDefaultCluster]
-
-	clientConfig.ConsulConfig = &sconfig.ConsulConfig{
-		Namespace: testNS,
-	}
+	clientConfig.ConsulConfigs = map[string]*sconfig.ConsulConfig{
+		structs.ConsulDefaultCluster: {
+			Namespace: testNS,
+		}}
 
 	// helper to reduce boilerplate
 	waitConfig := &config.WaitConfig{
@@ -2228,8 +2225,9 @@ func TestTaskTemplateManager_ClientTemplateConfig_Set(t *testing.T) {
 			},
 			&TaskTemplateManagerConfig{
 				ClientConfig: clientConfig,
+				ConsulConfig: clientConfig.GetDefaultConsul(),
 				VaultToken:   "token",
-				VaultConfig:  clientConfig.VaultConfigs[structs.VaultDefaultCluster],
+				VaultConfig:  clientConfig.GetDefaultVault(),
 				EnvBuilder:   taskenv.NewBuilder(clientConfig.Node, alloc, alloc.Job.TaskGroups[0].Tasks[0], clientConfig.Region),
 			},
 			&config.Config{
@@ -2262,8 +2260,9 @@ func TestTaskTemplateManager_ClientTemplateConfig_Set(t *testing.T) {
 			},
 			&TaskTemplateManagerConfig{
 				ClientConfig: clientConfig,
+				ConsulConfig: clientConfig.GetDefaultConsul(),
 				VaultToken:   "token",
-				VaultConfig:  clientConfig.VaultConfigs[structs.VaultDefaultCluster],
+				VaultConfig:  clientConfig.GetDefaultVault(),
 				EnvBuilder:   taskenv.NewBuilder(clientConfig.Node, allocWithOverride, allocWithOverride.Job.TaskGroups[0].Tasks[0], clientConfig.Region),
 			},
 			&config.Config{
@@ -2300,8 +2299,9 @@ func TestTaskTemplateManager_ClientTemplateConfig_Set(t *testing.T) {
 			},
 			&TaskTemplateManagerConfig{
 				ClientConfig: clientConfig,
+				ConsulConfig: clientConfig.GetDefaultConsul(),
 				VaultToken:   "token",
-				VaultConfig:  clientConfig.VaultConfigs[structs.VaultDefaultCluster],
+				VaultConfig:  clientConfig.GetDefaultVault(),
 				EnvBuilder:   taskenv.NewBuilder(clientConfig.Node, allocWithOverride, allocWithOverride.Job.TaskGroups[0].Tasks[0], clientConfig.Region),
 				Templates: []*structs.Template{
 					{
diff --git a/client/allocrunner/taskrunner/template_hook.go b/client/allocrunner/taskrunner/template_hook.go
index f8f7506f8..b993da44d 100644
--- a/client/allocrunner/taskrunner/template_hook.go
+++ b/client/allocrunner/taskrunner/template_hook.go
@@ -206,6 +206,10 @@ func (h *templateHook) newManager() (unblock chan struct{}, err error) {
 		}
 	}
 
+	tg := h.config.alloc.Job.LookupTaskGroup(h.config.alloc.TaskGroup)
+	consulCluster := h.task.GetConsulClusterName(tg)
+	consulConfig := h.config.clientConfig.GetConsulConfigs(h.logger)[consulCluster]
+
 	m, err := template.NewTaskTemplateManager(&template.TaskTemplateManagerConfig{
 		UnblockCh:            unblock,
 		Lifecycle:            h.config.lifecycle,
@@ -214,6 +218,7 @@ func (h *templateHook) newManager() (unblock chan struct{}, err error) {
 		ClientConfig:         h.config.clientConfig,
 		ConsulNamespace:      h.config.consulNamespace,
 		ConsulToken:          h.consulToken,
+		ConsulConfig:         consulConfig,
 		VaultToken:           h.vaultToken,
 		VaultConfig:          vaultConfig,
 		VaultNamespace:       h.vaultNamespace,
diff --git a/client/client.go b/client/client.go
index d3481a06c..cb2ffe4db 100644
--- a/client/client.go
+++ b/client/client.go
@@ -568,7 +568,7 @@ func NewClient(cfg *config.Config, consulCatalog consul.CatalogAPI, consulProxie
 	}
 
 	// Setup Consul discovery if enabled
-	if cfg.ConsulConfig.ClientAutoJoin != nil && *cfg.ConsulConfig.ClientAutoJoin {
+	if cfg.GetDefaultConsul().ClientAutoJoin != nil && *cfg.GetDefaultConsul().ClientAutoJoin {
 		c.shutdownGroup.Go(c.consulDiscovery)
 		if c.servers.NumServers() == 0 {
 			// No configured servers; trigger discovery manually
@@ -3014,7 +3014,7 @@ func taskIsPresent(taskName string, tasks []*structs.Task) bool {
 // triggerDiscovery causes a Consul discovery to begin (if one hasn't already)
 func (c *Client) triggerDiscovery() {
 	config := c.GetConfig()
-	if config.ConsulConfig.ClientAutoJoin != nil && *config.ConsulConfig.ClientAutoJoin {
+	if config.GetDefaultConsul() != nil && *config.GetDefaultConsul().ClientAutoJoin {
 		select {
 		case c.triggerDiscoveryCh <- struct{}{}:
 			// Discovery goroutine was released to execute
@@ -3059,7 +3059,7 @@ func (c *Client) consulDiscoveryImpl() error {
 		dcs = dcs[0:min(len(dcs), datacenterQueryLimit)]
 	}
 
-	serviceName := c.GetConfig().ConsulConfig.ServerServiceName
+	serviceName := c.GetConfig().GetDefaultConsul().ServerServiceName
 	var mErr multierror.Error
 	var nomadServers servers.Servers
 	consulLogger.Debug("bootstrap contacting Consul DCs", "consul_dcs", dcs)
diff --git a/client/config/config.go b/client/config/config.go
index 7fcbe10a9..151e5db7e 100644
--- a/client/config/config.go
+++ b/client/config/config.go
@@ -170,19 +170,11 @@ type Config struct {
 	// Version is the version of the Nomad client
 	Version *version.VersionInfo
 
-	// ConsulConfig is this Agent's default Consul configuration
-	ConsulConfig *structsc.ConsulConfig
-
 	// ConsulConfigs is a map of Consul configurations, here to support features
 	// in Nomad Enterprise. The default Consul config pointer above will be
 	// found in this map under the name "default"
 	ConsulConfigs map[string]*structsc.ConsulConfig
 
-	// VaultConfig is this Agent's default Vault configuration
-	//
-	// Deprecated: use GetVaultConfigs() instead.
-	VaultConfig *structsc.VaultConfig
-
 	// VaultConfigs is a map of Vault configurations, here to support features
 	// in Nomad Enterprise. The default Vault config pointer above will be found
 	// in this map under the name "default"
@@ -760,9 +752,7 @@ func (c *Config) Copy() *Config {
 	nc.Servers = slices.Clone(nc.Servers)
 	nc.Options = maps.Clone(nc.Options)
 	nc.HostVolumes = structs.CopyMapStringClientHostVolumeConfig(nc.HostVolumes)
-	nc.ConsulConfig = c.ConsulConfig.Copy()
 	nc.ConsulConfigs = helper.DeepCopyMap(c.ConsulConfigs)
-	nc.VaultConfig = c.VaultConfig.Copy()
 	nc.VaultConfigs = helper.DeepCopyMap(c.VaultConfigs)
 	nc.TemplateConfig = c.TemplateConfig.Copy()
 	nc.ReservableCores = slices.Clone(c.ReservableCores)
@@ -773,9 +763,11 @@ func (c *Config) Copy() *Config {
 // DefaultConfig returns the default configuration
 func DefaultConfig() *Config {
 	cfg := &Config{
-		Version:                 version.GetVersion(),
-		VaultConfig:             structsc.DefaultVaultConfig(),
-		ConsulConfig:            structsc.DefaultConsulConfig(),
+		Version: version.GetVersion(),
+		VaultConfigs: map[string]*structsc.VaultConfig{
+			structs.VaultDefaultCluster: structsc.DefaultVaultConfig()},
+		ConsulConfigs: map[string]*structsc.ConsulConfig{
+			structs.ConsulDefaultCluster: structsc.DefaultConsulConfig()},
 		Region:                  "global",
 		StatsCollectionInterval: 1 * time.Second,
 		TLSConfig:               &structsc.TLSConfig{},
@@ -815,11 +807,6 @@ func DefaultConfig() *Config {
 		MinDynamicPort:     structs.DefaultMaxDynamicPort,
 	}
 
-	cfg.ConsulConfigs = map[string]*structsc.ConsulConfig{
-		structs.ConsulDefaultCluster: cfg.ConsulConfig}
-	cfg.VaultConfigs = map[string]*structsc.VaultConfig{
-		structs.VaultDefaultCluster: cfg.VaultConfig}
-
 	return cfg
 }
 
@@ -960,3 +947,11 @@ func (c *Config) NomadPluginConfig(topology *numalib.Topology) *base.AgentConfig
 		},
 	}
 }
+
+func (c *Config) GetDefaultConsul() *structsc.ConsulConfig {
+	return c.ConsulConfigs[structs.ConsulDefaultCluster]
+}
+
+func (c *Config) GetDefaultVault() *structsc.VaultConfig {
+	return c.VaultConfigs[structs.VaultDefaultCluster]
+}
diff --git a/client/config/config_ce.go b/client/config/config_ce.go
index 3fd4593c4..ed1c86008 100644
--- a/client/config/config_ce.go
+++ b/client/config/config_ce.go
@@ -7,29 +7,26 @@ package config
 
 import (
 	"github.com/hashicorp/go-hclog"
-	"github.com/hashicorp/nomad/nomad/structs"
-	"github.com/hashicorp/nomad/nomad/structs/config"
 	structsc "github.com/hashicorp/nomad/nomad/structs/config"
 )
 
 // GetVaultConfigs returns the set of Vault configurations available for this
 // client. In Nomad CE we only use the default Vault.
 func (c *Config) GetVaultConfigs(logger hclog.Logger) map[string]*structsc.VaultConfig {
-	if c.VaultConfig == nil || !c.VaultConfig.IsEnabled() {
+	if c.VaultConfigs["default"] == nil || !c.VaultConfigs["default"].IsEnabled() {
 		return nil
 	}
 
 	if len(c.VaultConfigs) > 1 {
 		logger.Warn("multiple Vault configurations are only supported in Nomad Enterprise")
 	}
-
-	return map[string]*structsc.VaultConfig{structs.VaultDefaultCluster: c.VaultConfig}
+	return c.VaultConfigs
 }
 
 // GetConsulConfigs returns the set of Consul configurations the fingerprint needs
 // to check. In Nomad CE we only check the default Consul.
 func (c *Config) GetConsulConfigs(logger hclog.Logger) map[string]*structsc.ConsulConfig {
-	if c.ConsulConfig == nil {
+	if c.ConsulConfigs["default"] == nil {
 		return nil
 	}
 
@@ -37,5 +34,5 @@ func (c *Config) GetConsulConfigs(logger hclog.Logger) map[string]*structsc.Cons
 		logger.Warn("multiple Consul configurations are only supported in Nomad Enterprise")
 	}
 
-	return map[string]*config.ConsulConfig{structs.ConsulDefaultCluster: c.ConsulConfig}
+	return c.ConsulConfigs
 }
diff --git a/client/config/testing.go b/client/config/testing.go
index 156b5b54b..bff1e2e61 100644
--- a/client/config/testing.go
+++ b/client/config/testing.go
@@ -14,7 +14,6 @@ import (
 	"github.com/hashicorp/nomad/helper/pointer"
 	"github.com/hashicorp/nomad/helper/testlog"
 	"github.com/hashicorp/nomad/nomad/mock"
-	"github.com/hashicorp/nomad/nomad/structs"
 	testing "github.com/mitchellh/go-testing-interface"
 )
 
@@ -69,8 +68,7 @@ func TestClientConfig(t testing.T) (*Config, func()) {
 	// Helps make sure we are respecting configured parent
 	conf.CgroupParent = "testing.slice"
 
-	conf.VaultConfig.Enabled = pointer.Of(false)
-	conf.VaultConfigs[structs.VaultDefaultCluster].Enabled = pointer.Of(false)
+	conf.GetDefaultVault().Enabled = pointer.Of(false)
 	conf.DevMode = true
 
 	// Loosen GC threshold
diff --git a/client/fingerprint/consul_test.go b/client/fingerprint/consul_test.go
index 76bd197b9..3bc7db5fe 100644
--- a/client/fingerprint/consul_test.go
+++ b/client/fingerprint/consul_test.go
@@ -37,7 +37,7 @@ func fakeConsul(payload string) (*httptest.Server, *config.Config) {
 	}))
 
 	cfg := config.DefaultConfig()
-	cfg.ConsulConfig.Addr = strings.TrimPrefix(ts.URL, `http://`)
+	cfg.GetDefaultConsul().Addr = strings.TrimPrefix(ts.URL, `http://`)
 	return ts, cfg
 }
 
diff --git a/client/fingerprint/vault_test.go b/client/fingerprint/vault_test.go
index 8b033c015..15b573efc 100644
--- a/client/fingerprint/vault_test.go
+++ b/client/fingerprint/vault_test.go
@@ -34,7 +34,7 @@ func TestVaultFingerprint(t *testing.T) {
 	}
 
 	conf := config.DefaultConfig()
-	conf.VaultConfig = tv.Config
+	conf.VaultConfigs[structs.VaultDefaultCluster] = tv.Config
 
 	request := &FingerprintRequest{Config: conf, Node: node}
 	var response FingerprintResponse
diff --git a/client/gc_test.go b/client/gc_test.go
index 2d981796a..fa7ebdffb 100644
--- a/client/gc_test.go
+++ b/client/gc_test.go
@@ -378,7 +378,7 @@ func TestAllocGarbageCollector_MakeRoomFor_MaxAllocs(t *testing.T) {
 		c.GCInterval = time.Hour
 		c.RPCHandler = server
 		c.Servers = []string{serverAddr}
-		c.ConsulConfig.ClientAutoJoin = new(bool)
+		c.GetDefaultConsul().ClientAutoJoin = new(bool)
 	})
 	defer cleanup()
 	waitTilNodeReady(client, t)
diff --git a/command/agent/agent.go b/command/agent/agent.go
index 5516ee04a..e5dfbaeca 100644
--- a/command/agent/agent.go
+++ b/command/agent/agent.go
@@ -825,15 +825,9 @@ func convertClientConfig(agentConfig *Config) (*clientconfig.Config, error) {
 		return nil, fmt.Errorf("client_service_name must be set when auto_advertise is enabled")
 	}
 
-	conf.ConsulConfig = agentConfig.Consul
-	for _, consulConfig := range agentConfig.Consuls {
-		conf.ConsulConfigs[consulConfig.Name] = consulConfig
-	}
-
-	conf.VaultConfig = agentConfig.Vault
-	for _, vaultConfig := range agentConfig.Vaults {
-		conf.VaultConfigs[vaultConfig.Name] = vaultConfig
-	}
+	// Set the Vault and Consul configurations
+	conf.ConsulConfigs = agentConfig.Consuls
+	conf.VaultConfigs = agentConfig.Vaults
 
 	// Set up Telemetry configuration
 	conf.StatsCollectionInterval = agentConfig.Telemetry.collectionInterval
diff --git a/command/agent/consul/int_test.go b/command/agent/consul/int_test.go
index dfa6d200d..57c4657e6 100644
--- a/command/agent/consul/int_test.go
+++ b/command/agent/consul/int_test.go
@@ -66,9 +66,9 @@ func TestConsul_Integration(t *testing.T) {
 
 	conf := config.DefaultConfig()
 	conf.Node = mock.Node()
-	conf.ConsulConfig.Addr = testconsul.HTTPAddr
+	conf.GetDefaultConsul().Addr = testconsul.HTTPAddr
 	conf.APIListenerRegistrar = config.NoopAPIListenerRegistrar{}
-	consulConfig, err := conf.ConsulConfig.ApiConfig()
+	consulConfig, err := conf.GetDefaultConsul().ApiConfig()
 	if err != nil {
 		t.Fatalf("error generating consul config: %v", err)
 	}