Announcing the funding boost in his Spring statement, Chancellor Philip Hammond said the region had committed to delivering 215,000 homes by 2031.
It includes a £100m land and housing fund for the West Midlands Combined Authority (WMCA), which will deliver around 8,000 homes along the Walsall to Wolverhampton rail corridor.
The deal comes after ministers revealed plans to bring the line between the town and city back into use, including new railway stations at Willenhall and James Bridge, Darlaston.
The housing fund will focus on preparing brownfield sites for redevelopment across the Black Country, with Smethwick highlighted as a key priority.
It means the region will aim to build 16,000 homes a year, up from an average of 10,000 over the last three years.
West Midlands Mayor Andy Street, said the deal was 'a huge milestone' for the West Midlands that would help 'relieve pressure' on the greenbelt.
“Everybody acknowledges the housing challenges we face in this country," he added. "We have been clear with Government that here in the West Midlands we are a key part of the solution."
Councillor Sean Coughlan, leader of Walsall Council and the WMCA’s lead on housing and land, said: “As our economy continues to go from strength to strength, our population will increase so we will need to build more homes in the right places and ensure communities have access to employment.
“This deal will give us more tools to work with our partners and use innovative techniques to ensure delivery."
The West Midlands is the first region in the country to be handed cash from the Government's £4.1bn housing infrastructure fund, earmarked to unlock homes in areas of high demand.
Dudley South MP Mike Wood said: "Unless we build more houses, fewer and fewer young people locally will be able to have their own home.
"This investment gives them a better future, whilst making sure more houses are built on brownfield sites to reduce pressure on our valuable green spaces."
Ninder Johal, a board member at the Black Country Local Enterprise Partnership, said it was 'no surprise' that the West Midlands had landed the deal with the Government.
"This region is being recognised as the place to go, the place to live and the place to work," he said.
"It also comes with the recognition that we have a region that believes in collaboration and is getting better skilled and is both keen and committed to deliver.
"This builds on the fantastic work that our local enterprise partnerships and local councils have been putting in over the last year or so."
The cash will also support the Commonwealth Games Athletes’ village, as well as the creation of a new centre of excellence for brownfield remediation and construction skills in Wolverhampton.