diff --git a/.github/workflows/test.yml b/.github/workflows/test.yml
index 974c4f859c..59361edb26 100644
--- a/.github/workflows/test.yml
+++ b/.github/workflows/test.yml
@@ -163,6 +163,29 @@ jobs:
         run: |
           make -o build validate-${{ matrix.script }}
 
+  validate-api-swagger:
+    runs-on: ubuntu-24.04
+    timeout-minutes: 10 # guardrails timeout for the whole job
+    defaults:
+      run:
+        working-directory: api
+    needs:
+      - validate-dco
+    name: validate (api-swagger)
+    steps:
+      -
+        name: Checkout
+        uses: actions/checkout@v4
+      - 
+        name: Build api module image
+        run: |
+          make build GO_VERSION=${{ env.GO_VERSION }}
+      - 
+        name: Validate swagger
+        run: |
+          make validate-swagger
+          make validate-swagger-gen
+
   smoke-prepare:
     runs-on: ubuntu-24.04
     timeout-minutes: 10 # guardrails timeout for the whole job
diff --git a/Dockerfile b/Dockerfile
index 00efb68815..89de8e5858 100644
--- a/Dockerfile
+++ b/Dockerfile
@@ -83,22 +83,6 @@ RUN --mount=type=cache,sharing=locked,id=moby-criu-aptlib,target=/var/lib/apt \
 FROM distribution/distribution:$REGISTRY_VERSION AS registry
 RUN mkdir /build && mv /bin/registry /build/registry
 
-# go-swagger
-FROM base AS swagger
-WORKDIR /go/src/github.com/go-swagger/go-swagger
-ARG TARGETPLATFORM
-# GO_SWAGGER_VERSION specifies the version of the go-swagger binary to install.
-# Go-swagger is used in CI for generating types from swagger.yaml in
-# hack/validate/swagger-gen
-ARG GO_SWAGGER_VERSION=v0.33.1
-RUN --mount=type=cache,target=/root/.cache/go-build,id=swagger-build-$TARGETPLATFORM \
-    --mount=type=cache,target=/go/pkg/mod \
-    --mount=type=tmpfs,target=/go/src/ <<EOT
-  set -e
-  GOBIN=/build CGO_ENABLED=0 xx-go install "github.com/go-swagger/go-swagger/cmd/swagger@${GO_SWAGGER_VERSION}"
-  xx-verify /build/swagger
-EOT
-
 # frozen-images
 # See also frozenImages in "testutil/environment/protect.go" (which needs to
 # be updated when adding images to this list)
@@ -420,7 +404,6 @@ FROM docker/compose-bin:${COMPOSE_VERSION} AS compose
 
 FROM base AS dev-systemd-false
 COPY --link --from=frozen-images /build/ /docker-frozen-images
-COPY --link --from=swagger       /build/ /usr/local/bin/
 COPY --link --from=delve         /build/ /usr/local/bin/
 COPY --link --from=gowinres      /build/ /usr/local/bin/
 COPY --link --from=tini          /build/ /usr/local/bin/
diff --git a/Makefile b/Makefile
index 532a691408..ac2b39c534 100644
--- a/Makefile
+++ b/Makefile
@@ -118,11 +118,8 @@ DELVE_PORT_FORWARD := $(if $(DELVE_PORT),-p "$(DELVE_PORT)",)
 
 DOCKER_FLAGS := $(DOCKER) run --rm --privileged $(DOCKER_CONTAINER_NAME) $(DOCKER_ENVS) $(DOCKER_MOUNT) $(DOCKER_PORT_FORWARD) $(DELVE_PORT_FORWARD)
 
-SWAGGER_DOCS_PORT ?= 9000
-
 define \n
 
-
 endef
 
 # if this session isn't interactive, then we don't want to allocate a
@@ -263,20 +260,12 @@ win: bundles ## cross build the binary for windows
 	$(BAKE_CMD) --set *.platform=windows/amd64 binary
 
 .PHONY: swagger-gen
-swagger-gen:
-	docker run --rm -v $(PWD):/go/src/github.com/docker/docker \
-		-w /go/src/github.com/docker/docker \
-		--entrypoint hack/generate-swagger-api.sh \
-		-e GOPATH=/go \
-		quay.io/goswagger/swagger:0.7.4
+swagger-gen:  ## generate swagger API types
+	$(MAKE) -C api swagger-gen
 
 .PHONY: swagger-docs
 swagger-docs: ## preview the API documentation
-	@echo "API docs preview will be running at http://localhost:$(SWAGGER_DOCS_PORT)"
-	@docker run --rm -v $(PWD)/api/swagger.yaml:/usr/share/nginx/html/swagger.yaml \
-		-e 'REDOC_OPTIONS=hide-hostname="true" lazy-rendering' \
-		-p $(SWAGGER_DOCS_PORT):80 \
-		bfirsh/redoc:1.14.0
+	$(MAKE) -C api swagger-docs
 
 .PHONY: generate-files
 generate-files:
diff --git a/api/Dockerfile b/api/Dockerfile
new file mode 100644
index 0000000000..85e2920dd9
--- /dev/null
+++ b/api/Dockerfile
@@ -0,0 +1,25 @@
+# syntax=docker/dockerfile:1
+
+ARG GO_VERSION=1.25.4
+
+FROM golang:${GO_VERSION}-alpine AS base
+RUN apk add --no-cache bash make yamllint
+CMD ["/bin/bash"]
+
+# go-swagger
+FROM base AS swagger
+WORKDIR /go/src/github.com/go-swagger/go-swagger
+# GO_SWAGGER_VERSION specifies the version of the go-swagger binary to install.
+# Go-swagger is used in CI for generating types from swagger.yaml in
+# api/scripts/generate-swagger-api.sh
+ARG GO_SWAGGER_VERSION=v0.33.1
+ARG TARGETPLATFORM
+RUN --mount=type=cache,target=/root/.cache/go-build,id=swagger-build-$TARGETPLATFORM \
+    --mount=type=cache,target=/go/pkg/mod \
+    CGO_ENABLED=0 go install "github.com/go-swagger/go-swagger/cmd/swagger@${GO_SWAGGER_VERSION}" && \
+    /go/bin/swagger version
+
+# dev is a dev-environment to work with the api module.
+FROM base AS dev
+COPY --from=swagger /go/bin/swagger /usr/local/bin/swagger
+WORKDIR /go/src/github.com/moby/moby/api
diff --git a/api/Makefile b/api/Makefile
new file mode 100644
index 0000000000..33b8ee78da
--- /dev/null
+++ b/api/Makefile
@@ -0,0 +1,64 @@
+# API Module Makefile
+# This Makefile provides targets for the swagger generation and validation
+# which are specific to the API module.
+
+DOCKER ?= docker
+BUILDX ?= $(DOCKER) buildx
+
+API_DIR := $(CURDIR)
+PROJECT_PATH := /go/src/github.com/moby/moby
+
+DOCKER_MOUNT := -v "$(API_DIR):$(PROJECT_PATH)/api"
+
+DOCKER_IMAGE := docker-api-dev
+
+DOCKER_WORKDIR := -w $(PROJECT_PATH)/api
+
+DOCKER_FLAGS := $(DOCKER) run --rm $(DOCKER_MOUNT) $(DOCKER_WORKDIR)
+DOCKER_RUN := $(DOCKER_FLAGS) "$(DOCKER_IMAGE)"
+
+DOCKER_CONTAINER_NAME := $(if $(CONTAINER_NAME),--name $(CONTAINER_NAME),)
+
+BUILD_CMD := $(BUILDX) build
+GO_VERSION ?= 1.25.4
+SWAGGER_VERSION ?= v0.33.1
+SWAGGER_DOCS_PORT ?= 9000
+
+.DEFAULT_GOAL := help
+
+.PHONY: build
+build:
+	$(BUILD_CMD) \
+		--build-arg GO_VERSION=$(GO_VERSION) \
+		--build-arg SWAGGER_VERSION=$(SWAGGER_VERSION) \
+		--target dev \
+		--load \
+		-t "$(DOCKER_IMAGE)" \
+		-f Dockerfile \
+		.
+
+.PHONY: swagger-gen
+swagger-gen: build ## generate swagger API types
+	$(DOCKER_RUN) ./scripts/generate-swagger-api.sh
+
+.PHONY: swagger-docs
+swagger-docs: ## preview the API documentation
+	@echo "API docs preview will be running at http://localhost:$(SWAGGER_DOCS_PORT)"
+	@docker run --rm \
+		-v $(PWD)/:/usr/share/nginx/html/swagger/ \
+		-e 'REDOC_OPTIONS=hide-hostname="true" lazy-rendering' \
+		-e SPEC_URL="swagger/swagger.yaml" \
+		-p $(SWAGGER_DOCS_PORT):80 \
+		redocly/redoc:v2.5.1
+
+.PHONY: validate-swagger
+validate-swagger: build ## validate the swagger.yaml file
+	$(DOCKER_RUN) ./scripts/validate-swagger.sh
+
+.PHONY: validate-swagger-gen
+validate-swagger-gen: build ## validate generated types are up-to-date
+	$(DOCKER_RUN) ./scripts/validate-swagger-gen.sh
+
+.PHONY: help
+help: ## display this help message
+	@awk 'BEGIN {FS = ":.*?## "} /^[a-zA-Z0-9_-]+:.*?## / {printf "\033[36m%-20s\033[0m %s\n", $$1, $$2}' $(MAKEFILE_LIST)
diff --git a/hack/generate-swagger-api.sh b/api/scripts/generate-swagger-api.sh
similarity index 82%
rename from hack/generate-swagger-api.sh
rename to api/scripts/generate-swagger-api.sh
index 7fedb8ff9a..205614b860 100755
--- a/hack/generate-swagger-api.sh
+++ b/api/scripts/generate-swagger-api.sh
@@ -3,24 +3,26 @@
 # -*- indent-tabs-mode: t -*-
 set -eu
 
+API_DIR="$(cd "$(dirname "${BASH_SOURCE[0]}")/.." && pwd)"
+
 generate_model() {
 	local package="$1"
 	shift
 	mapfile
-	swagger generate model --spec=api/swagger.yaml \
-		--target=api --model-package="$package" \
-		--config-file=api/swagger-gen.yaml \
-		--template-dir=api/templates --allow-template-override \
+	swagger generate model --spec="${API_DIR}/swagger.yaml" \
+		--target="${API_DIR}" --model-package="$package" \
+		--config-file="${API_DIR}/swagger-gen.yaml" \
+		--template-dir="${API_DIR}/templates" --allow-template-override \
 		"$@" \
 		$(printf -- '--name=%s ' "${MAPFILE[@]}")
 }
 
 generate_operation() {
 	mapfile
-	swagger generate operation --spec=api/swagger.yaml \
-		--target=api --api-package=types --model-package=types \
-		--config-file=api/swagger-gen.yaml \
-		--template-dir=api/templates --allow-template-override \
+	swagger generate operation --spec="${API_DIR}/swagger.yaml" \
+		--target="${API_DIR}" --api-package=types --model-package=types \
+		--config-file="${API_DIR}/swagger-gen.yaml" \
+		--template-dir="${API_DIR}/templates" --allow-template-override \
 		"$@" \
 		$(printf -- '--name=%s ' "${MAPFILE[@]}")
 }
diff --git a/api/scripts/validate-swagger-gen.sh b/api/scripts/validate-swagger-gen.sh
new file mode 100755
index 0000000000..781b807ec0
--- /dev/null
+++ b/api/scripts/validate-swagger-gen.sh
@@ -0,0 +1,52 @@
+#!/usr/bin/env bash
+set -euo pipefail
+
+SCRIPT_DIR="$(cd "$(dirname "${BASH_SOURCE[0]}")" && pwd)"
+API_DIR="${SCRIPT_DIR}/.."
+
+TMP_DIR="$(mktemp -d)"
+trap "rm -rf ${TMP_DIR}" EXIT
+GEN_FILES=()
+
+echo "Validating generated code..."
+echo "Separating generated files from handwritten files..."
+while IFS= read -r file; do
+	GEN_FILES+=("$file")
+done < <(grep -rl "// Code generated" "${API_DIR}/types" || true)
+
+echo "Copying generated files into temporary folder..."
+for f in "${GEN_FILES[@]}"; do
+	mkdir -p "${TMP_DIR}/$(dirname "${f#${API_DIR}/}")"
+	cp "$f" "${TMP_DIR}/${f#${API_DIR}/}"
+done
+
+cp "${API_DIR}/swagger.yaml" "${TMP_DIR}/"
+cp "${API_DIR}/swagger-gen.yaml" "${TMP_DIR}/"
+cp -r "${API_DIR}/templates" "${TMP_DIR}/" 2> /dev/null || true
+
+echo "Generating swagger types in temporary folder..."
+(
+	cd "${TMP_DIR}"
+	"${SCRIPT_DIR}/generate-swagger-api.sh" > /dev/null 2>&1
+)
+
+echo "Run diff for all generated files..."
+DIFF_FOUND=false
+for f in "${GEN_FILES[@]}"; do
+	REL="${f#${API_DIR}/}"
+	if ! diff -q "${TMP_DIR}/${REL}" "${API_DIR}/${REL}" > /dev/null 2>&1; then
+		echo "Difference found in ${REL}"
+		diff -u "${TMP_DIR}/${REL}" "${API_DIR}/${REL}" || true
+		DIFF_FOUND=true
+	fi
+done
+
+if [ "$DIFF_FOUND" = true ]; then
+	echo
+	echo "Swagger validation failed. Please run:"
+	echo "  ./scripts/generate-swagger-api.sh"
+	echo "and commit updated generated files."
+	exit 1
+fi
+
+echo "Swagger file is up to date."
diff --git a/api/scripts/validate-swagger.sh b/api/scripts/validate-swagger.sh
new file mode 100755
index 0000000000..b129be7ed6
--- /dev/null
+++ b/api/scripts/validate-swagger.sh
@@ -0,0 +1,16 @@
+#!/usr/bin/env bash
+set -e
+
+# Expected to be in api directory
+cd "$(dirname "${BASH_SOURCE[0]}")/.."
+
+echo "Validating swagger.yaml..."
+
+yamllint -f parsable -c validate/yamllint.yaml swagger.yaml
+
+if out=$(swagger validate swagger.yaml); then
+	echo "Validation done! ${out}"
+else
+	echo "${out}" >&2
+	false
+fi
diff --git a/hack/validate/yamllint b/api/validate/yamllint
similarity index 100%
rename from hack/validate/yamllint
rename to api/validate/yamllint
diff --git a/hack/validate/yamllint.yaml b/api/validate/yamllint.yaml
similarity index 100%
rename from hack/validate/yamllint.yaml
rename to api/validate/yamllint.yaml
diff --git a/hack/validate/swagger b/hack/validate/swagger
deleted file mode 100755
index 5313221b7b..0000000000
--- a/hack/validate/swagger
+++ /dev/null
@@ -1,18 +0,0 @@
-#!/usr/bin/env bash
-set -e
-SCRIPTDIR="$(cd "$(dirname "${BASH_SOURCE[0]}")" && pwd)"
-source "${SCRIPTDIR}/.validate"
-
-IFS=$'\n'
-files=($(validate_diff --diff-filter=ACMR --name-only -- 'api/swagger.yaml' || true))
-unset IFS
-
-if [ -n "${TEST_FORCE_VALIDATE:-}" ] || [ ${#files[@]} -gt 0 ]; then
-	yamllint -f parsable -c "${SCRIPTDIR}"/yamllint.yaml api/swagger.yaml
-	if out=$(swagger validate api/swagger.yaml); then
-		echo "Congratulations!  ${out}"
-	else
-		echo "${out}" >&2
-		false
-	fi
-fi
diff --git a/hack/validate/swagger-gen b/hack/validate/swagger-gen
deleted file mode 100755
index 40631703cd..0000000000
--- a/hack/validate/swagger-gen
+++ /dev/null
@@ -1,29 +0,0 @@
-#!/usr/bin/env bash
-
-SCRIPTDIR="$(cd "$(dirname "${BASH_SOURCE[0]}")" && pwd)"
-source "${SCRIPTDIR}/.validate"
-
-IFS=$'\n'
-files=($(validate_diff --diff-filter=ACMR --name-only -- 'api/types/' 'api/swagger.yaml' || true))
-unset IFS
-
-if [ -n "${TEST_FORCE_VALIDATE:-}" ] || [ ${#files[@]} -gt 0 ]; then
-	"${SCRIPTDIR}"/../generate-swagger-api.sh 2> /dev/null
-	# Let see if the working directory is clean
-	diffs="$(git diff -- api/types/)"
-	if [ "$diffs" ]; then
-		{
-			echo 'The result of hack/generate-swagger-api.sh differs'
-			echo
-			echo "$diffs"
-			echo
-			echo 'Please update api/swagger.yaml with any API changes, then '
-			echo 'run hack/generate-swagger-api.sh.'
-		} >&2
-		false
-	else
-		echo 'Congratulations!  All API changes are done the right way.'
-	fi
-else
-	echo 'No api/types/ or api/swagger.yaml changes in diff.'
-fi