diff --git a/.changeset/engine-strict-devengines-runtime.md b/.changeset/engine-strict-devengines-runtime.md
new file mode 100644
index 0000000000..e8bf0066b0
--- /dev/null
+++ b/.changeset/engine-strict-devengines-runtime.md
@@ -0,0 +1,6 @@
+---
+"@pnpm/config": patch
+"pnpm": patch
+---
+
+Engine validation now uses the Node.js version from `devEngines.runtime` (or `engines.runtime`) instead of the system Node.js version [#10033](https://github.com/pnpm/pnpm/issues/10033).
diff --git a/config/config/src/index.ts b/config/config/src/index.ts
index e451c10130..a3f9463630 100644
--- a/config/config/src/index.ts
+++ b/config/config/src/index.ts
@@ -402,6 +402,9 @@ export async function getConfig (opts: {
       if (pnpmConfig.rootProjectManifest) {
         Object.assign(pnpmConfig, getOptionsFromRootManifest(pnpmConfig.rootProjectManifestDir, pnpmConfig.rootProjectManifest))
       }
+      if (pnpmConfig.nodeVersion == null) {
+        pnpmConfig.nodeVersion = getNodeVersionFromEnginesRuntime(pnpmConfig.rootProjectManifest)
+      }
     }
 
     if (pnpmConfig.workspaceDir != null) {
@@ -721,6 +724,21 @@ function parseDevEnginesPackageManager (devEngines?: DevEngines): EngineDependen
   }
 }
 
+function getNodeVersionFromEnginesRuntime (manifest: ProjectManifest): string | undefined {
+  for (const enginesFieldName of ['devEngines', 'engines'] as const) {
+    const enginesRuntime = manifest[enginesFieldName]?.runtime
+    if (enginesRuntime == null) continue
+    const runtimes: EngineDependency[] = Array.isArray(enginesRuntime) ? enginesRuntime : [enginesRuntime]
+    const nodeRuntime = runtimes.find((r) => r.name === 'node')
+    if (nodeRuntime?.version == null) continue
+    const minVersion = semver.minVersion(nodeRuntime.version)
+    if (minVersion != null) {
+      return minVersion.version
+    }
+  }
+  return undefined
+}
+
 function addSettingsFromWorkspaceManifestToConfig (pnpmConfig: Config, {
   configFromCliOpts,
   projectManifest,
diff --git a/config/config/test/index.ts b/config/config/test/index.ts
index bf9b186be1..0172e1c892 100644
--- a/config/config/test/index.ts
+++ b/config/config/test/index.ts
@@ -56,6 +56,57 @@ test('getConfig()', async () => {
   expect(config.nodeVersion).toBeUndefined()
 })
 
+test.each([
+  { field: 'devEngines' as const, version: '22.20.0', onFail: 'download' as const, expected: '22.20.0' },
+  { field: 'devEngines' as const, version: '22.20.0', onFail: 'error' as const, expected: '22.20.0' },
+  { field: 'devEngines' as const, version: '^22.0.0', onFail: 'download' as const, expected: '22.0.0' },
+  { field: 'engines' as const, version: '22.20.0', onFail: 'download' as const, expected: '22.20.0' },
+])('when $field is $version and onFail is $onFail, nodeVersion is set to $expected', async ({ field, version, onFail, expected }) => {
+  prepare({
+    [field]: {
+      runtime: {
+        name: 'node',
+        version,
+        onFail,
+      },
+    },
+  })
+
+  const { config } = await getConfig({
+    cliOptions: {},
+    packageManager: {
+      name: 'pnpm',
+      version: '1.0.0',
+    },
+  })
+
+  expect(config.nodeVersion).toBe(expected)
+})
+
+test('nodeVersion from config takes priority over devEngines.runtime', async () => {
+  prepare({
+    devEngines: {
+      runtime: {
+        name: 'node',
+        version: '22.20.0',
+        onFail: 'download',
+      },
+    },
+  })
+
+  const { config } = await getConfig({
+    cliOptions: {
+      'node-version': '20.0.0',
+    },
+    packageManager: {
+      name: 'pnpm',
+      version: '1.0.0',
+    },
+  })
+
+  expect(config.nodeVersion).toBe('20.0.0')
+})
+
 test('throw error if --link-workspace-packages is used with --global', async () => {
   await expect(getConfig({
     cliOptions: {