Prime Minister Boris Johnson said the 2.5 million tenants renting their homes from housing associations will be given the right to buy them outright under plans to extend the policy.
But critics say it risks further reducing social housing stock, with housing charity Shelter describing the plan as "reckless".
Councils are expected to replace these homes on a one-for-one basis, but just 83 replacements were acquired or began construction in the area over this period.
Right to Buy was introduced in 1980 to help council and housing association tenants buy their home, at a discount of up to £87,200 outside London.
Mr Johnson sought to move on from the recent confidence vote and Partygate scandal with a major policy speech in Blackpool, which focussed on how the Government will address the cost-of-living crisis.
In it, he said ministers would seek to ease the pain of soaring interest rates by working to “finish the right-to-own reforms Margaret Thatcher began in the 1980s” and extending the Right to Buy scheme to those “trapped” in their housing association homes.
He criticised some associations for showing “scandalous indifference” to tenants and pledged a one-for-one replacement of each property sold to prevent the housing stock dwindling in an attempt to address the major criticism of his Tory predecessor’s policy.
Across England, 96,100 homes have been sold through Right to Buy since 2012-13, with just 32,900 replacement houses acquired or started.
Alicia Walker, head of policy, research and campaigns at homeless charity Centrepoint, said: "Extending the Right to Buy to housing associations risks further eroding the stock of social housing, which many young people desperately need.
"Promises of like-for-like replacements have been made before but not been followed through.”
Mr Johnson also announced a change to welfare rules so that the 1.5 million people who are in work but also on housing benefit will have the choice to use their benefit towards a mortgage.
But Shelter described the Prime Minister's Right to Buy and “benefits to bricks” policies as "baffling, unworkable, and a dangerous gimmick".
Polly Neate, chief executive of Shelter, said: “Hatching reckless plans to extend Right to Buy will put our rapidly shrinking supply of social homes at even greater risk.
“The maths doesn’t add up: why try to sell off what little truly affordable housing is left – at great expense – when homelessness is rising and over a million households are stuck on the waiting list?
“The Government needs to stop wasting time on the failed policies of the past and start building more of the secure social homes this country actually needs.”
The MHCLG figures show that Chesterfield Council collected £32 million through the Right to Buy scheme over nine years.