This will be the first office outside of London with a regular ministerial presence.
At least 500 ministry roles are set to be based across the West Midlands by 2025, with further increases planned by 2030.
Senior civil servants will also be based in Wolverhampton, ensuring this becomes a centre for policy development and decision making.
This is a significant rise on the 300 roles currently in the region and is part of plans to have at least 800 roles outside of London by 2030 — including half of the most senior positions.
This decision was made to ensure that more local voices are reflected in the creation of government policy.
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It also aims to help provide an economic boost to the area and offer improved career paths outside of Whitehall.
Recruitment is already underway, with 40 roles already relocated to the region in the last 12 months.
The government expects to announce the new building for the headquarters in the spring.
“As communities secretary, I am determined to spread opportunity and prosperity to every part of our nation,” said Jenrick.
“With a dual headquarters in Wolverhampton, my department will not only change where we work, but how we work, signalling the end of the Whitehall-knows-best approach.
“In choosing the city of Wolverhampton, we are also backing our great, smaller cities, some of which have been neglected for too long.
“We want to raise their stature, encourage civic pride and commercial success.”