A swathe of government buildings and public housing will be sold over four years, raising $400 million for the city to Gungahlin tram line.
The sale will hit 1356 tenants as the government takes advantage of the federal asset recycling payment scheme.
Well known buildings will go on the market, including the health building in Moore Street, the Motor Registry, Dame Pattie Menzies House and the ambulance station in Dickson and Macarthur House and the visitor centre on Northbourne Avenue.
The government wouldn't say which properties will be sold first but sales are due to be completed by 2019.
Public housing around the city will be sold, including the Red Hill flats, Strathgordon Court on Melrose Drive in Woden, the Stuart flats in Griffith, the Allawah, Bega and Currong apartments and the Northbourne flats and housing precinct, part of which has just been given heritage protection.
In all, the buildings contain 1216 flats and are home to 1356 tenants.
The Northbourne flats and housing precinct have 403 units, home to 557 people. Another 313 tenants live in the 440 "ABC flats" in the city, with the Currong block already vacated. The Red Hill units house 239 tenants, the Stuart flats 157 and Strathgordon Court 90.
The sale was revealed by Treasurer Joe Hockey as he signed a deal with Chief Minister Andrew Barr on Thursday, which will see the territory receive about $60 million in bonuses under the Commonwealth scheme designed to encourage states to sell assets.
The $105 million sale of betting agency ACTTAB has attracted a bonus payment of $15.8 million.
The documents have blanked out the timing of sales and the expected sale prices, but reveal that 100 per cent of the amount made will go to the $783 million tram project from Gungahlin to the city.
The health building on the corner of Moore and Alinga streets is currently home to a host of health services, including a dental program and a breast screening centre, as well as the Asbestos Taskforce and the Act Civil and Administrative Appeals Tribunal.
The Enivornment and Planning Directorate and ACT Planning and Land Authority is based in Dame Pattie Menzies House, while Macarthur House is home to the ACT government's Territory and Municipal Services Directorate.
Under the terms of the deal the territory is required to ensure the total stock of public housing does not fall below June 2014 levels of 10,848 dwellings.
Mr Hockey's announcement explains Mr Barr's scathing attack on the heritage listing, which he described on Wednesday as "absurd", declaring the government would push ahead with plans to demolish the flats and sell the land for the development of 1100 apartments in their place.
State and territory governments are eligible for a 15 percent bonus from the Commonwealth for agreed asset sales under the scheme.
Mr Hockey said the ACT was the first to sign up to the scheme and confirmed all the funds would go to the Capital Metro light rail project. He described the 12-kilometre tram line to Gungahlin as "controversial".
The Abbott government has previously said it would not fund public transport projects, in favour of national roads funding.
"While the project was considered to meet the criteria of the [asset recycling] initiative, the Commonwealth is aware that there has been debate as to whether alternative projects may have higher potential economic benefits," Mr Hockey said.
Previously Infrastructure Australia has declined to fund the tram line.
"As the territory's renewal of public housing progresses and outdated accommodation is replaced roof-for-roof, surplus land will be sold under the scheme and attract further bonuses," Mr Barr said.
Opposition planning spokesman Alistair Coe said the government was "squandering a Commonwealth cash bonus on light rail".
"It is unfortunate that the only infrastructure project the ACT government nominated is light rail," he said.
"The Coalition government's gift to the ACT could have been spent on any number of projects, such as road upgrades, bus infrastructure, or a convention centre. However, given the ACT has no such projects planned, light rail was the only option."