Housing and planning minister Alok Sharma has announced that the Planning Delivery Fund is open for bids.
Councils will be able to apply to help gain the skills or capacity they need to deliver housing growth at scale and implement wider planning reforms.
Mr Sharma said: “Locally led developments have enormous potential to deliver the scale and quality of housing growth that we need.
“By supporting our local authorities, we will be able to unlock more homes where people want to live.
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“These measures include the £25m of government support which will help develop new communities that will not only help deliver high-quality, well-designed homes, but will also bring new jobs and facilities and a boost to local economies.”
In the Autumn Budget last month, the chancellor Philip Hammond announced the government has committed at least £44bn of funding to support the housing market.
Alongside the fund, a further £3m has been earmarked to support the delivery of 14 garden villages.
There are currently 24 locally led garden cities, towns and villages with the potential to deliver around 220,000 homes.