The development of the site, which fronts Challis Street in Dickson and backs on to Northbourne Avenue, is the second signal this week that the government is under way with its ambitious plans to remake Northbourne Avenue.

Demolition of the Dickson Towers began this week, the first of the historic public housing to go to make way for redevelopment and to raise money for the planned light rail line.

The government is selling a swathe of public housing and other buildings along the route, including Macarthur House and the the tourist visitors' centre, hoping to reinvent it as a zone of high-density living and commercial activity, fed by trams and private developments nearby.

A tram and bus interchange will also be located in Dickson, at the end of Cape Street beside the motor registry site. In October, the government compulsorily acquired a section of land for the interchange. The acquisition is finalised but no compensation claim has been lodged by the former owners, a Taiwanese family company registered in Sydney.

The call for registrations of interest for the Dickson motor registry site was published on Saturday.

Chief Minister Andrew Barr said the land was being offered to a developer to build a government office block, as well as other commercial and residential developments opportunities.

The government would commit to lease about 13,000 square metres of office space in the new building, including for a new Access Canberra shopfront and yet-to-be-determined government directorate staff.

Mr Barr said the redevelopment of Northbourne Avenue would create jobs and stimulate the territory economy. The ACT's largest renewal of public housing is under way and Mr Barr said the plans would see Northbourne become "a vibrant boulevard that welcomes visitors to the national capital".

The motor registry building was well past its useful economic life, Mr Barr said.

The vehicle checking station would be relocated to Hume, and the motor registry and other staff would move by the time the site was sold to developers.

The registration of interest call asks developers to prepare a concept plan for the site, with registrations closing at the end of March. A shortlist would be chosen and invited to tender for the project, with a developer chosen by the government by July.

The registry building is among those being sold to raise money for the tram project, under the federal asset recycling scheme, which gives 15 per cent cash incentives to state and territory governments to promote asset sales.

Funds for the scheme have to be spent on the light rail project and the ACT government is bound by a 2019 deadline.