A key slice of land on Northbourne Avenue is up for sale, with the site of the former Macarthur House expected to yield more than 400 apartments.
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The block has come onto the market almost two years after demolition of the former ACT public service offices began.
It is being sold via a tender and a minimum reserve price has been disclosed at $19 million.
Buildings on the site could be up to 35 metres high. A developer would be required to submit a tender which allowed for a 750-square-metre supermarket on site and other parts are required for community use.
Fifty affordable dwellings are another requirement of the tender.
The sale of the office block was flagged in the ACT's 2017 budget and was expected to be sold in the 2018/19 financial year.
A spokesman from the Suburban Land Agency said the sale was delayed because of amendments to the planning code, which directly impacted on the site.
The planning controls are governed by the City and Gateway Framework. Amendments to the Territory Plan and the National Capital Plan have been made to allow this framework.
"Suburban Land Agency wanted to ensure more certainty around planning controls on the site and transparency of controls to this site," a spokesman said.
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The City and Gateway Framework, unveiled in 2018, would pave the way for the construction of 37,000 new dwellings.
The sale of Macarthur House forms part of the Commonwealth's asset recycling scheme, in which the government received bonuses for selling off old buildings.
The Suburban Land agency spokesman said the block had been identified as an "important node" on Northbourne Avenue.
"Under the city and gateway framework this was always identified as a precinct of great opportunity for increasing its prominence and being right on a light rail stop as well, there's a real opportunity to create a a new precinct," he said.
As part of the tender, the Suburban Land Agency spokesman said an applicant would have to fulfil a range of design and quality requirements.
Developers that put in an application and propose a price less than the $19 million reserve would not be considered, the spokesman said.
The tender is being managed by JLL and Colliers International and applications will close on August 13.
The settlement date is not expected until March 31 next year.