diff --git a/.github/workflows/dogfood.yaml b/.github/workflows/dogfood.yaml
index b039ccc37f..2bd0e6d29f 100644
--- a/.github/workflows/dogfood.yaml
+++ b/.github/workflows/dogfood.yaml
@@ -11,15 +11,19 @@ on:
   #   PRs: `build_image` builds the image variants but never pushes
   #   (each `depot/build-push-action` step's `push:` and the
   #   `Push Nix image` step are gated on `github.ref ==
-  #   'refs/heads/main'`). `deploy_template` runs `terraform init` +
-  #   `validate` only; the apply step and SHA/title gathering are
-  #   gated on main.
+  #   'refs/heads/main'`). `test_image` rebuilds the Ubuntu images
+  #   from Depot cache with `load: true` and runs `make gen`, `fmt`,
+  #   `lint`, and a Linux build inside each image to validate that
+  #   the baked-in tooling works. `deploy_template` runs
+  #   `terraform init` + `validate` only; the apply step and
+  #   SHA/title gathering are gated on main.
   #
   #   Pushes to main: `build_image` retags rolling tags on
   #   `codercom/oss-dogfood` (`:latest`, `:22.04`, `:26.04`),
   #   `codercom/oss-dogfood-vscode-coder` (`:latest`), and
   #   `codercom/oss-dogfood-nix` (`:latest`), plus a per-branch tag on
-  #   each. `deploy_template` runs `terraform apply` and creates new
+  #   each. `test_image` validates tooling as above.
+  #   `deploy_template` runs `terraform apply` and creates new
   #   `coderd_template` versions on dev.coder.com whose `name` is the
   #   commit short SHA. Content is unchanged when neither `dogfood/**`
   #   nor the flake files changed, so the new versions are cosmetic.
@@ -31,12 +35,16 @@ on:
       - ".github/workflows/dogfood.yaml"
       - "flake.lock"
       - "flake.nix"
+      - "mise.toml"
+      - "mise.lock"
   pull_request:
     paths:
       - "dogfood/**"
       - ".github/workflows/dogfood.yaml"
       - "flake.lock"
       - "flake.nix"
+      - "mise.toml"
+      - "mise.lock"
   workflow_dispatch:
 
 permissions:
@@ -193,8 +201,59 @@ jobs:
         env:
           DOCKER_TAG: ${{ steps.docker-tag-name.outputs.tag }}
 
-  deploy_template:
+  # Validate that the Ubuntu dogfood images contain working tooling.
+  # Failures here block template deployment (deploy_template).
+  test_image:
     needs: build_image
+    strategy:
+      fail-fast: false
+      matrix:
+        image-version: ["22.04", "26.04"]
+    runs-on: ${{ github.repository_owner == 'coder' && 'depot-ubuntu-22.04-8' || 'ubuntu-latest' }}
+    steps:
+      - name: Harden Runner
+        uses: step-security/harden-runner@f808768d1510423e83855289c910610ca9b43176 # v2.17.0
+        with:
+          egress-policy: audit
+
+      - name: Checkout
+        uses: actions/checkout@de0fac2e4500dabe0009e67214ff5f5447ce83dd # v6.0.2
+        with:
+          fetch-depth: 1
+          persist-credentials: false
+
+      - name: Set up Depot CLI
+        uses: depot/setup-action@15c09a5f77a0840ad4bce955686522a257853461 # v1.7.1
+
+      - name: Set up Docker Buildx
+        uses: docker/setup-buildx-action@4d04d5d9486b7bd6fa91e7baf45bbb4f8b9deedd # v4.0.0
+
+      # Near-instant cache hit from build_image; loads into local daemon
+      # without pushing to a registry.
+      - name: Load dogfood image from Depot cache
+        uses: depot/build-push-action@5f3b3c2e5a00f0093de47f657aeaefcedff27d18 # v1.17.0
+        with:
+          project: b4q6ltmpzh
+          token: ${{ secrets.DEPOT_TOKEN }}
+          buildx-fallback: true
+          context: "{{defaultContext}}"
+          file: dogfood/coder/ubuntu-${{ matrix.image-version }}/Dockerfile
+          secrets: |
+            github_token=${{ secrets.GITHUB_TOKEN }}
+          pull: true
+          load: true
+          push: false
+          tags: "dogfood-test:${{ matrix.image-version }}"
+
+      - name: Test image tooling
+        run: ./scripts/dogfood_test_image.sh "dogfood-test:${{ matrix.image-version }}"
+        env:
+          GITHUB_TOKEN: ${{ secrets.GITHUB_TOKEN }}
+
+  deploy_template:
+    needs:
+      - build_image
+      - test_image
     runs-on: ubuntu-latest
     permissions:
       # Necessary for GCP authentication (https://github.com/google-github-actions/setup-gcloud#usage)
diff --git a/Makefile b/Makefile
index f07c8ee35a..5b8af71bb2 100644
--- a/Makefile
+++ b/Makefile
@@ -992,7 +992,10 @@ GEN_FILES := \
 	$(AIBRIDGED_MOCKS)
 
 # all gen targets should be added here and to gen/mark-fresh
-gen: gen/db gen/golden-files $(GEN_FILES)
+# Set GEN_SKIP_GOLDEN=1 to skip gen/golden-files (which needs Docker to
+# start PostgreSQL via testcontainers).
+GEN_SKIP_GOLDEN ?=
+gen: gen/db $(if $(GEN_SKIP_GOLDEN),,gen/golden-files) $(GEN_FILES)
 .PHONY: gen
 
 gen/db: $(DB_GEN_FILES)
diff --git a/scripts/dogfood_test_image.sh b/scripts/dogfood_test_image.sh
new file mode 100755
index 0000000000..08360d7511
--- /dev/null
+++ b/scripts/dogfood_test_image.sh
@@ -0,0 +1,107 @@
+#!/usr/bin/env bash
+
+# Validates dogfood image tooling by running gen, fmt, lint, and build inside
+# the image. Can be run locally or in CI (mirrors the test_image workflow job).
+#
+# Usage: ./scripts/dogfood_test_image.sh <image>
+#
+# Arguments:
+#   image   Docker image to test, e.g. dogfood-test:22.04 or
+#           ghcr.io/coder/dogfood:latest
+#
+# Environment:
+#   GITHUB_TOKEN      Passed into the container for authenticated API calls
+#                     (optional for local runs).
+#   GITHUB_BASE_REF   Base branch for diff-only lint checks (e.g. emdash).
+#                     Set automatically by GitHub Actions for PRs.
+#   CI                When set, fmt targets run in check-mode and actionlint
+#                     is excluded from make lint (it runs separately in CI).
+#   STEPS             Space-separated list of steps to run. Defaults to all.
+#                     Valid values: gen fmt lint build check-unstaged
+#
+# Example:
+#   ./scripts/dogfood_test_image.sh dogfood-test:22.04
+#   STEPS="gen fmt" ./scripts/dogfood_test_image.sh dogfood-test:26.04
+
+set -euo pipefail
+# shellcheck source=scripts/lib.sh
+source "$(dirname "${BASH_SOURCE[0]}")/lib.sh"
+cdroot
+
+if [[ $# -lt 1 ]]; then
+	echo "Usage: $0 <image>" >&2
+	exit 1
+fi
+
+IMAGE="$1"
+STEPS="${STEPS:-gen fmt lint build check-unstaged}"
+
+log() {
+	echo "==> $*" >&2
+}
+
+# --- setup -------------------------------------------------------------------
+
+if [[ -n "${CI:-}" ]]; then
+	log "Preparing checkout for container user (UID 1000)"
+	chmod -R a+rwX .
+else
+	log "NOTE: if the container cannot write to the checkout, run: chmod -R a+rwX ."
+fi
+
+# Helper: run a make target inside the image.
+# Caches are persisted in named Docker volumes so that subsequent steps (and
+# repeated local runs) reuse downloaded modules and compiled artifacts.
+run_make() {
+	docker run --rm \
+		--volume "$(pwd)":/home/coder/coder \
+		--env GIT_CONFIG_COUNT=1 \
+		--env GIT_CONFIG_KEY_0=safe.directory \
+		--env GIT_CONFIG_VALUE_0=/home/coder/coder \
+		--volume coder-dogfood-gomod:/home/coder/go/pkg/mod \
+		--volume coder-dogfood-gobuild:/home/coder/.cache/go-build \
+		--volume coder-dogfood-pnpm:/home/coder/.local/share/pnpm/store \
+		--workdir /home/coder/coder \
+		--network=host \
+		--env GITHUB_TOKEN \
+		--env GITHUB_BASE_REF \
+		--env CI \
+		"$IMAGE" \
+		make "$@"
+}
+
+# --- steps -------------------------------------------------------------------
+
+for step in $STEPS; do
+	case "$step" in
+	gen)
+		log "make gen (GEN_SKIP_GOLDEN=1, skips tests that need Docker/testcontainers)"
+		run_make --output-sync=line -j gen GEN_SKIP_GOLDEN=1
+		;;
+	fmt)
+		log "make fmt"
+		run_make --output-sync=line -j fmt
+		;;
+	lint)
+		log "make lint"
+		run_make --output-sync=line -j lint
+		;;
+	build)
+		log "make build (fat binary)"
+		run_make -j build/coder_linux_amd64
+		;;
+	check-unstaged)
+		# Runs on the host: inspects git state after container steps wrote
+		# generated/formatted files back via the volume mount.
+		log "Checking for unstaged files"
+		./scripts/check_unstaged.sh
+		;;
+	*)
+		echo "Unknown step: $step" >&2
+		echo "Valid steps: gen fmt lint build check-unstaged" >&2
+		exit 1
+		;;
+	esac
+done
+
+log "All steps passed."