diff --git a/changelog/26427.txt b/changelog/26427.txt
new file mode 100644
index 0000000000..615e9e15f0
--- /dev/null
+++ b/changelog/26427.txt
@@ -0,0 +1,3 @@
+```release-note:bug
+agent: `vault.namespace` no longer gets incorrectly overridden by `auto_auth.namespace`, if set
+```
diff --git a/command/agent.go b/command/agent.go
index cc86bc051c..7bab660ce3 100644
--- a/command/agent.go
+++ b/command/agent.go
@@ -328,6 +328,9 @@ func (c *AgentCommand) Run(args []string) int {
 			client.SetNamespace(config.AutoAuth.Method.Namespace)
 		}
 		templateNamespace = client.Namespace()
+		if !namespaceSetByEnvironmentVariable && config.Vault != nil && config.Vault.Namespace != "" {
+			templateNamespace = config.Vault.Namespace
+		}
 
 		sinkClient, err := client.CloneWithHeaders()
 		if err != nil {