diff --git a/api/allocations.go b/api/allocations.go
index 9bd2d7aa656..2d859ffcc95 100644
--- a/api/allocations.go
+++ b/api/allocations.go
@@ -148,9 +148,6 @@ func (a *Allocations) GC(alloc *Allocation, q *QueryOptions) error {
 // Note: for cluster topologies where API consumers don't have network access to
 // Nomad clients, set api.ClientConnTimeout to a small value (ex 1ms) to avoid
 // long pauses on this API call.
-//
-// BREAKING: This method will have the following signature in 1.6.0
-// func (a *Allocations) Restart(allocID string, taskName string, allTasks bool, w *WriteOptions) (*WriteMeta, error) {
 func (a *Allocations) Restart(alloc *Allocation, taskName string, q *QueryOptions) error {
 	req := AllocationRestartRequest{
 		TaskName: taskName,
@@ -223,9 +220,6 @@ type AllocStopResponse struct {
 // Note: for cluster topologies where API consumers don't have network access to
 // Nomad clients, set api.ClientConnTimeout to a small value (ex 1ms) to avoid
 // long pauses on this API call.
-//
-// BREAKING: This method will have the following signature in 1.6.0
-// func (a *Allocations) Signal(allocID string, task string, signal string, w *WriteOptions) (*WriteMeta, error) {
 func (a *Allocations) Signal(alloc *Allocation, q *QueryOptions, task, signal string) error {
 	req := AllocSignalRequest{
 		Signal: signal,
diff --git a/api/api.go b/api/api.go
index af960745d81..107457ce146 100644
--- a/api/api.go
+++ b/api/api.go
@@ -937,9 +937,8 @@ func (c *Client) query(endpoint string, out any, q *QueryOptions) (*QueryMeta, e
 	return qm, nil
 }
 
-// putQuery is used to do a PUT request when doing a read against an endpoint
-// and deserialize the response into an interface using standard Nomad
-// conventions.
+// putQuery is used to do a PUT request when doing a "write" to a Client RPC.
+// Client RPCs must use QueryOptions to allow setting AllowStale=true.
 func (c *Client) putQuery(endpoint string, in, out any, q *QueryOptions) (*QueryMeta, error) {
 	r, err := c.newRequest("PUT", endpoint)
 	if err != nil {
@@ -969,6 +968,31 @@ func (c *Client) put(endpoint string, in, out any, q *WriteOptions) (*WriteMeta,
 	return c.write(http.MethodPut, endpoint, in, out, q)
 }
 
+// postQuery is used to do a POST request when doing a "write" to a Client RPC.
+// Client RPCs must use QueryOptions to allow setting AllowStale=true.
+func (c *Client) postQuery(endpoint string, in, out any, q *QueryOptions) (*QueryMeta, error) {
+	r, err := c.newRequest("POST", endpoint)
+	if err != nil {
+		return nil, err
+	}
+	r.setQueryOptions(q)
+	r.obj = in
+	rtt, resp, err := requireOK(c.doRequest(r))
+	if err != nil {
+		return nil, err
+	}
+	defer resp.Body.Close()
+
+	qm := &QueryMeta{}
+	parseQueryMeta(resp, qm)
+	qm.RequestTime = rtt
+
+	if err := decodeBody(resp, out); err != nil {
+		return nil, err
+	}
+	return qm, nil
+}
+
 // post is used to do a POST request against an endpoint and
 // serialize/deserialized using the standard Nomad conventions.
 func (c *Client) post(endpoint string, in, out any, q *WriteOptions) (*WriteMeta, error) {
diff --git a/api/node_meta.go b/api/node_meta.go
index be851206bf7..4d5c4ffa590 100644
--- a/api/node_meta.go
+++ b/api/node_meta.go
@@ -30,9 +30,9 @@ func (n *Nodes) Meta() *NodeMeta {
 
 // Apply dynamic Node metadata updates to a Node. If NodeID is unset then Node
 // receiving the request is modified.
-func (n *NodeMeta) Apply(meta *NodeMetaApplyRequest, qo *WriteOptions) (*NodeMetaResponse, error) {
+func (n *NodeMeta) Apply(meta *NodeMetaApplyRequest, qo *QueryOptions) (*NodeMetaResponse, error) {
 	var out NodeMetaResponse
-	_, err := n.client.post("/v1/client/metadata", meta, &out, qo)
+	_, err := n.client.postQuery("/v1/client/metadata", meta, &out, qo)
 	if err != nil {
 		return nil, err
 	}
diff --git a/command/agent/meta_endpoint.go b/command/agent/meta_endpoint.go
index f07fe014a47..28250554944 100644
--- a/command/agent/meta_endpoint.go
+++ b/command/agent/meta_endpoint.go
@@ -59,7 +59,7 @@ func (s *HTTPServer) nodeMetaApply(resp http.ResponseWriter, req *http.Request)
 		return nil, CodedError(http.StatusBadRequest, err.Error())
 	}
 
-	s.parseWriteRequest(req, &args.WriteRequest)
+	s.parse(resp, req, &args.QueryOptions.Region, &args.QueryOptions)
 	parseNode(req, &args.NodeID)
 
 	// Determine the handler to use
diff --git a/contributing/checklist-rpc-endpoint.md b/contributing/checklist-rpc-endpoint.md
index f8df1c0c8e7..a961d8ca00c 100644
--- a/contributing/checklist-rpc-endpoint.md
+++ b/contributing/checklist-rpc-endpoint.md
@@ -42,6 +42,14 @@ Prefer adding a new message to changing any existing RPC messages.
     upgraded, so use this to guard sending the new RPC, else send the old RPC
   * Version must match the actual release version!
 
+* [ ] If implementing a Client RPC...
+  * Use `QueryOptions` instead of `WriteRequest` in the Request struct as
+    `WriteRequest` is only for *Raft* writes.
+  * Set `QueryOptions.AllowStale = true` in the *Server* RPC forwarder to avoid
+    an infinite loop between leaders and followers when a Client RPC is
+    forwarded through a follower. See
+    https://github.com/hashicorp/nomad/issues/16517
+
 ## Docs
 
 * [ ] Changelog
diff --git a/nomad/client_meta_endpoint.go b/nomad/client_meta_endpoint.go
index 80c7d237b77..1795a6abad0 100644
--- a/nomad/client_meta_endpoint.go
+++ b/nomad/client_meta_endpoint.go
@@ -25,6 +25,10 @@ func newNodeMetaEndpoint(srv *Server) *NodeMeta {
 func (n *NodeMeta) Apply(args *structs.NodeMetaApplyRequest, reply *structs.NodeMetaResponse) error {
 	const method = "NodeMeta.Apply"
 
+	// Prevent infinite loop between leader and
+	// follower-with-the-target-node-connection.
+	args.QueryOptions.AllowStale = true
+
 	authErr := n.srv.Authenticate(nil, args)
 	if done, err := n.srv.forward(method, args, args, reply); done {
 		return err
@@ -48,6 +52,10 @@ func (n *NodeMeta) Apply(args *structs.NodeMetaApplyRequest, reply *structs.Node
 func (n *NodeMeta) Read(args *structs.NodeSpecificRequest, reply *structs.NodeMetaResponse) error {
 	const method = "NodeMeta.Read"
 
+	// Prevent infinite loop between leader and
+	// follower-with-the-target-node-connection.
+	args.QueryOptions.AllowStale = true
+
 	authErr := n.srv.Authenticate(nil, args)
 	if done, err := n.srv.forward(method, args, args, reply); done {
 		return err
diff --git a/nomad/structs/node.go b/nomad/structs/node.go
index f930b3385af..f025335ec94 100644
--- a/nomad/structs/node.go
+++ b/nomad/structs/node.go
@@ -357,7 +357,7 @@ func (di *DriverInfo) HealthCheckEquals(other *DriverInfo) bool {
 
 // NodeMetaApplyRequest is used to update Node metadata on Client agents.
 type NodeMetaApplyRequest struct {
-	WriteRequest
+	QueryOptions // Client RPCs must use QueryOptions to set AllowStale=true
 
 	// NodeID is the node being targeted by this request (or the node
 	// receiving this request if NodeID is empty).