diff --git a/.server-changes/supervisor-pod-dns-ndots.md b/.server-changes/supervisor-pod-dns-ndots.md
new file mode 100644
index 0000000000..48d3563f14
--- /dev/null
+++ b/.server-changes/supervisor-pod-dns-ndots.md
@@ -0,0 +1,8 @@
+---
+area: supervisor
+type: feature
+---
+
+Add `KUBERNETES_POD_DNS_NDOTS_OVERRIDE_ENABLED` flag (off by default) that overrides the cluster default and sets `dnsConfig.options.ndots` on runner pods (defaulting to 2, configurable via `KUBERNETES_POD_DNS_NDOTS`). Kubernetes defaults pods to `ndots: 5`, so any name with fewer than 5 dots — including typical external domains like `api.example.com` — is first walked through every entry in the cluster search list (`<ns>.svc.cluster.local`, `svc.cluster.local`, `cluster.local`) before being tried as-is, turning one resolution into 4+ CoreDNS queries (×2 with A+AAAA). Using a lower `ndots` value reduces DNS query amplification in the `cluster.local` zone.
+
+Note: before enabling, make sure no code path relies on search-list expansion for names with dots ≥ the configured value — those names will hit their as-is form first and could resolve externally before falling back to the cluster search path.
diff --git a/apps/supervisor/src/env.ts b/apps/supervisor/src/env.ts
index b69fb24d73..f2d54741ee 100644
--- a/apps/supervisor/src/env.ts
+++ b/apps/supervisor/src/env.ts
@@ -121,6 +121,16 @@ const Env = z
 
     KUBERNETES_MEMORY_OVERHEAD_GB: z.coerce.number().min(0).optional(), // Optional memory overhead to add to the limit in GB
     KUBERNETES_SCHEDULER_NAME: z.string().optional(), // Custom scheduler name for pods
+
+    // Pod DNS config — override the cluster default ndots to `KUBERNETES_POD_DNS_NDOTS`.
+    // Default k8s ndots is 5: any name with fewer than 5 dots (e.g. `api.example.com`, 2 dots) is first walked
+    // through every entry in the cluster search list (`<ns>.svc.cluster.local`, `svc.cluster.local`, `cluster.local`)
+    // before being tried as-is, turning one resolution into 4+ CoreDNS queries (×2 with A+AAAA).
+    // Overriding the default can be useful to cut CoreDNS query amplification for external domains.
+    // Note: before enabling, make sure no code path relies on search-list expansion for names with dots ≥ the value
+    // set here — those names will now hit their as-is form first and could resolve externally before falling back.
+    KUBERNETES_POD_DNS_NDOTS_OVERRIDE_ENABLED: BoolEnv.default(false),
+    KUBERNETES_POD_DNS_NDOTS: z.coerce.number().int().min(1).max(15).default(2),
     // Large machine affinity settings - large-* presets prefer a dedicated pool
     KUBERNETES_LARGE_MACHINE_AFFINITY_ENABLED: BoolEnv.default(false),
     KUBERNETES_LARGE_MACHINE_AFFINITY_POOL_LABEL_KEY: z
@@ -189,7 +199,9 @@ const Env = z
             if (!validEffects.includes(effect)) {
               ctx.addIssue({
                 code: z.ZodIssueCode.custom,
-                message: `Invalid toleration effect "${effect}" in "${entry}". Must be one of: ${validEffects.join(", ")}`,
+                message: `Invalid toleration effect "${effect}" in "${entry}". Must be one of: ${validEffects.join(
+                  ", "
+                )}`,
               });
               return z.NEVER;
             }
diff --git a/apps/supervisor/src/workloadManager/kubernetes.ts b/apps/supervisor/src/workloadManager/kubernetes.ts
index ec08926721..b2ed05c9f1 100644
--- a/apps/supervisor/src/workloadManager/kubernetes.ts
+++ b/apps/supervisor/src/workloadManager/kubernetes.ts
@@ -321,6 +321,13 @@ export class KubernetesWorkloadManager implements WorkloadManager {
             },
           }
         : {}),
+      ...(env.KUBERNETES_POD_DNS_NDOTS_OVERRIDE_ENABLED
+        ? {
+            dnsConfig: {
+              options: [{ name: "ndots", value: `${env.KUBERNETES_POD_DNS_NDOTS}` }],
+            },
+          }
+        : {}),
     };
   }