diff --git a/.changelog/27167.txt b/.changelog/27167.txt
new file mode 100644
index 00000000000..9a005b5da1c
--- /dev/null
+++ b/.changelog/27167.txt
@@ -0,0 +1,3 @@
+```release-note:bug
+server: Fix a potential race condition when reloading the server agent when changing TLS configuration
+```
diff --git a/nomad/rpc.go b/nomad/rpc.go
index d2e7a359f13..4a997aa2b32 100644
--- a/nomad/rpc.go
+++ b/nomad/rpc.go
@@ -301,8 +301,8 @@ func (r *rpcHandler) handleConn(ctx context.Context, conn net.Conn, rpcCtx *RPCC
 	}
 
 	// Enforce TLS if EnableRPC is set
-	if r.srv.config.TLSConfig.EnableRPC && !rpcCtx.TLS && pool.RPCType(buf[0]) != pool.RpcTLS {
-		if !r.srv.config.TLSConfig.RPCUpgradeMode {
+	if r.srv.rpcTLSEnabled.Load() && !rpcCtx.TLS && pool.RPCType(buf[0]) != pool.RpcTLS {
+		if !r.srv.rpcTLSUpgradeMode.Load() {
 			r.logger.Warn("non-TLS connection attempted with RequireTLS set", "remote_addr", conn.RemoteAddr())
 			conn.Close()
 			return
diff --git a/nomad/server.go b/nomad/server.go
index 912bc2c1b22..5ac3b7af8b4 100644
--- a/nomad/server.go
+++ b/nomad/server.go
@@ -105,8 +105,22 @@ const (
 // Server is Nomad server which manages the job queues,
 // schedulers, and notification bus for agents.
 type Server struct {
+
+	// config holds the server configuration. No fields are not mutated after
+	// initialization except for the TLS config, so it is safe to access them
+	// without a lock. Any fields that become reloadable, must be carefully
+	// assessed for concurrent access.
 	config *Config
 
+	// rpcTLSEnabled and rpcTLSUpgradeMode are used by the RPC connection
+	// handler to determine TLS enforcement. The values can change at runtime
+	// due to config reloading.
+	//
+	// The setRPCTLSAtomics helper function should be used to set these values
+	// as it correctly handles nil configs.
+	rpcTLSEnabled     atomic.Bool
+	rpcTLSUpgradeMode atomic.Bool
+
 	logger log.InterceptLogger
 
 	// Connection pool to other Nomad servers
@@ -350,6 +364,8 @@ func NewServer(config *Config, consulCatalog consul.CatalogAPI, consulConfigFunc
 	// Create the server
 	s := &Server{
 		config:                  config,
+		rpcTLSEnabled:           atomic.Bool{},
+		rpcTLSUpgradeMode:       atomic.Bool{},
 		consulCatalog:           consulCatalog,
 		connPool:                pool.NewPool(logger, serverRPCCache, serverMaxStreams, tlsWrap, config.RPCSessionConfig),
 		logger:                  logger,
@@ -372,6 +388,10 @@ func NewServer(config *Config, consulCatalog consul.CatalogAPI, consulConfigFunc
 		lockDelayTimer:          lock.NewDelayTimer(),
 	}
 
+	// Store the server TLS RPC settings that will be used by the connection
+	// handler.
+	s.setRPCTLSAtomics(config.TLSConfig)
+
 	s.shutdownCtx, s.shutdownCancel = context.WithCancel(context.Background())
 	s.shutdownCh = s.shutdownCtx.Done()
 
@@ -690,16 +710,19 @@ func (s *Server) reloadTLSConnections(newTLSConfig *config.TLSConfig) error {
 	s.tlsWrap = tlsWrap
 	s.tlsWrapLock.Unlock()
 
-	// Keeping configuration in sync is important for other places that require
-	// access to config information, such as rpc.go, where we decide on what kind
-	// of network connections to accept depending on the server configuration
+	// Ensure the config object is updated. This is done to keep things in sync
+	// only; all access to TLS enforcement should be done via the atomics which
+	// are updated below.
 	s.config.TLSConfig = newTLSConfig
 
+	// Update the RPC TLS atomics used for connection handling.
+	s.setRPCTLSAtomics(newTLSConfig)
+
 	// Kill any old listeners
 	s.rpcCancel()
 
 	// Update the authenticator, so any changes in TLS verification are applied.
-	s.auth.SetVerifyTLS(s.config.TLSConfig != nil && s.config.TLSConfig.EnableRPC && s.config.TLSConfig.VerifyServerHostname)
+	s.auth.SetVerifyTLS(s.config.TLSConfig != nil && s.rpcTLSEnabled.Load() && s.config.TLSConfig.VerifyServerHostname)
 
 	s.rpcTLS = incomingTLS
 	s.connPool.ReloadTLS(tlsWrap)
@@ -2088,6 +2111,16 @@ func (s *Server) setReplyQueryMeta(stateStore *state.StateStore, table string, r
 	return nil
 }
 
+// setRPCTLSAtomics is a helper function to set the atomic values for RPC TLS
+// handling based on the provided config.
+//
+// This should be used whenever the RPC TLS config is changed to ensure as it
+// correctly handles nil configs which might otherwise be missed.
+func (s *Server) setRPCTLSAtomics(cfg *config.TLSConfig) {
+	s.rpcTLSEnabled.Store(cfg != nil && cfg.EnableRPC)
+	s.rpcTLSUpgradeMode.Store(cfg != nil && cfg.RPCUpgradeMode)
+}
+
 // Region returns the region of the server
 func (s *Server) Region() string {
 	return s.config.Region
diff --git a/nomad/server_test.go b/nomad/server_test.go
index ea490c6e48b..2a933b6fcfa 100644
--- a/nomad/server_test.go
+++ b/nomad/server_test.go
@@ -9,6 +9,7 @@ import (
 	"path"
 	"runtime"
 	"strings"
+	"sync/atomic"
 	"testing"
 	"time"
 
@@ -441,7 +442,7 @@ func TestServer_Reload_TLSConnections_PlaintextToTLS_OnlyRPC(t *testing.T) {
 
 	err := s1.reloadTLSConnections(newTLSConfig)
 	assert.Nil(err)
-	assert.True(s1.config.TLSConfig.EnableRPC)
+	must.True(t, s1.rpcTLSEnabled.Load())
 	assert.True(s1.config.TLSConfig.CertificateInfoIsEqual(newTLSConfig))
 
 	codec := rpcClient(t, s1)
@@ -702,3 +703,30 @@ func TestServer_PreventRaftDowngrade(t *testing.T) {
 	// Downgrading Raft should prevent the server from starting.
 	require.Error(t, err)
 }
+
+func TestServer_setRPCTLSAtomics(t *testing.T) {
+	ci.Parallel(t)
+
+	testServer := &Server{
+		rpcTLSEnabled:     atomic.Bool{},
+		rpcTLSUpgradeMode: atomic.Bool{},
+	}
+
+	testServer.setRPCTLSAtomics(nil)
+	must.False(t, testServer.rpcTLSEnabled.Load())
+	must.False(t, testServer.rpcTLSUpgradeMode.Load())
+
+	testServer.setRPCTLSAtomics(&config.TLSConfig{
+		EnableRPC:      true,
+		RPCUpgradeMode: false,
+	})
+	must.True(t, testServer.rpcTLSEnabled.Load())
+	must.False(t, testServer.rpcTLSUpgradeMode.Load())
+
+	testServer.setRPCTLSAtomics(&config.TLSConfig{
+		EnableRPC:      true,
+		RPCUpgradeMode: true,
+	})
+	must.True(t, testServer.rpcTLSEnabled.Load())
+	must.True(t, testServer.rpcTLSUpgradeMode.Load())
+}