diff --git a/.buildkite/pipelines/pull-request-transport-versions.yml b/.buildkite/pipelines/pull-request-transport-versions.yml
index c8030c3bbc887..d4d3ecc12898d 100644
--- a/.buildkite/pipelines/pull-request-transport-versions.yml
+++ b/.buildkite/pipelines/pull-request-transport-versions.yml
@@ -1 +1,10 @@
-steps: []
+steps:
+  - label: update-transport-versions
+    command: '.buildkite/scripts/update-transport-versions.sh'
+    # New transport versions are always added via the main branch
+    if: build.env('BUILDKITE_PULL_REQUEST_BASE_BRANCH') == 'main'
+    agents:
+      provider: gcp
+      image: family/elasticsearch-ubuntu-2404
+      machineType: custom-16-32768
+      buildDirectory: /dev/shm/bk
diff --git a/.buildkite/scripts/update-transport-versions.sh b/.buildkite/scripts/update-transport-versions.sh
new file mode 100755
index 0000000000000..c3ae067f9ce9a
--- /dev/null
+++ b/.buildkite/scripts/update-transport-versions.sh
@@ -0,0 +1,51 @@
+#!/bin/bash
+set -euo pipefail
+
+if [[ -z "${BUILDKITE_PULL_REQUEST:-}" ]]; then
+  echo "Not a pull request, skipping transport version update"
+  exit 0
+fi
+
+if ! git diff --exit-code; then
+  echo "Changes are present before updating transport versions, not running"
+  git status
+  exit 0
+fi
+
+NEW_COMMIT_MESSAGE="[CI] Update transport version definitions"
+
+echo "--- Generating updated transport version definitions"
+# Calculate backport branches based on pull request version labels
+backport_branches=$(
+  echo "${GITHUB_PR_LABELS}" \
+    | tr ',' '\n' \
+    | grep -E "v[0-9]+\.[0-9]+\.[0-9]+" \
+    | sed -E 's/^v([0-9]+)\.([0-9]+)\.[0-9]+$/\1.\2/' \
+    | paste -sd, -
+)
+
+if [[ -z "${backport_branches}" ]]; then
+  echo "Skipping as pull request contains no version labels"
+  exit 0
+fi
+
+.ci/scripts/run-gradle.sh generateTransportVersion --backport-branches="${backport_branches}"
+
+if git diff --exit-code; then
+  echo "No changes found after updating transport versions. Don't need to auto commit."
+  exit 0
+fi
+
+git config --global user.name elasticsearchmachine
+git config --global user.email 'infra-root+elasticsearchmachine@elastic.co'
+
+gh pr checkout "${BUILDKITE_PULL_REQUEST}"
+git add -A .
+git commit -m "$NEW_COMMIT_MESSAGE"
+git push
+
+# After the git push, the new commit will trigger a new build within a few seconds and this build should get cancelled
+# So, let's just sleep to give the build time to cancel itself without an error
+# If it doesn't get cancelled for some reason, then exit with an error, because we don't want this build to be green (we just don't want it to generate an error either)
+sleep 300
+exit 1