diff --git a/dcrwallet.go b/dcrwallet.go
index 7013e9462..6d54dcda5 100644
--- a/dcrwallet.go
+++ b/dcrwallet.go
@@ -370,7 +370,7 @@ func run(ctx context.Context) error {
 	//
 	// Servers will be associated with a loaded wallet if it has already been
 	// loaded, or after it is loaded later on.
-	gRPCServer, jsonRPCServer, err := startRPCServers(loader)
+	gRPCServer, jsonRPCServer, err := startRPCServers(ctx, loader)
 	if err != nil {
 		log.Errorf("Unable to create RPC servers: %v", err)
 		return err
diff --git a/internal/rpc/jsonrpc/server.go b/internal/rpc/jsonrpc/server.go
index 7f43675c4..8e7cd37f6 100644
--- a/internal/rpc/jsonrpc/server.go
+++ b/internal/rpc/jsonrpc/server.go
@@ -1,5 +1,5 @@
 // Copyright (c) 2013-2015 The btcsuite developers
-// Copyright (c) 2017-2019 The Decred developers
+// Copyright (c) 2017-2024 The Decred developers
 // Use of this source code is governed by an ISC
 // license that can be found in the LICENSE file.
 
@@ -91,13 +91,20 @@ func jsonAuthFail(w http.ResponseWriter) {
 
 // NewServer creates a new server for serving JSON-RPC client connections,
 // both HTTP POST and websocket.
-func NewServer(opts *Options, activeNet *chaincfg.Params, walletLoader *loader.Loader, listeners []net.Listener) *Server {
+func NewServer(ctx context.Context, opts *Options, activeNet *chaincfg.Params, walletLoader *loader.Loader, listeners []net.Listener) *Server {
 	serveMux := http.NewServeMux()
 	const rpcAuthTimeoutSeconds = 10
 	server := &Server{
 		httpServer: http.Server{
 			Handler: serveMux,
 
+			// Use the provided context as the parent context for all requests
+			// to ensure handlers are able to react to both client disconnects
+			// as well as shutdown via the provided context.
+			BaseContext: func(l net.Listener) context.Context {
+				return ctx
+			},
+
 			// Timeout connections which don't complete the initial
 			// handshake within the allowed timeframe.
 			ReadTimeout: time.Second * rpcAuthTimeoutSeconds,
diff --git a/rpcserver.go b/rpcserver.go
index 6e3870f90..7076a00b0 100644
--- a/rpcserver.go
+++ b/rpcserver.go
@@ -229,7 +229,7 @@ func generateClientKeyPair(caPriv any, ca *x509.Certificate) (cert, key []byte,
 	return cert, key, nil
 }
 
-func startRPCServers(walletLoader *loader.Loader) (*grpc.Server, *jsonrpc.Server, error) {
+func startRPCServers(ctx context.Context, walletLoader *loader.Loader) (*grpc.Server, *jsonrpc.Server, error) {
 	var jsonrpcAddrNotifier jsonrpcListenerEventServer
 	var grpcAddrNotifier grpcListenerEventServer
 	if cfg.RPCListenerEvents {
@@ -367,7 +367,7 @@ func startRPCServers(walletLoader *loader.Loader) (*grpc.Server, *jsonrpc.Server
 			TicketSplitAccount:  cfg.TicketSplitAccount,
 			Dial:                cfg.dial,
 		}
-		jsonrpcServer = jsonrpc.NewServer(&opts, activeNet.Params, walletLoader, listeners)
+		jsonrpcServer = jsonrpc.NewServer(ctx, &opts, activeNet.Params, walletLoader, listeners)
 		for _, lis := range listeners {
 			jsonrpcAddrNotifier.notify(lis.Addr().String())
 		}