The ACT government is testing the market for more office space in the city, as it consolidates the territory's public service in Civic and Dickson.
About 2700 public servants are set to move into office blocks currently under construction in the two areas.
The Challis Street and Constitution Avenue blocks are due to be finished in late 2020.
But the territory government has also called for expressions of interest to provide more office space in the heart of Canberra.
"For various functional and operational reasons, there are a number of work groups which will not be accommodated in the new buildings," tender documents released on Thursday state.
The government's preference is for most of the office space - approximately 7000 to 9000 square metres - to be in one building in the central business district.
However it will consider splitting the required space across multiple buildings if its requirements can't be satisfied with one site.
For example, the government requires between 1300 and 1500 square metres of ground floor space close to transport and Civic's retail precinct for customer service areas and meeting rooms.
Some of the agencies may be "best suited" to separate accommodation of less than 1000 square metres, it said.
"Although the general aim will be to consolidate the number of leases and reduce the overall space requirement through shared facilities, the result will depend on the location, quality and cost of the properties offered for lease in response to this [request for expressions of interest]," the tender reads.
The new office space would need to be fitted out and ready for tenants by October 1, 2020.
It would be leased for 10 years, with an option to extend the lease for another five years.
The properties would have to have a minimum 4.5-star energy rating - five stars if it was a new building - and "comprehensive" end-of-trip, "wellness" and bicycle storage facilities.
The tender is part of a 2016 plan to revitalise Canberra's town centres by consolidating 1700 public servants in Civic, 1000 in Dickson and 1100 in Woden.
Off the back of concerns about vacant office space in the city, the government planned to lease 20,000 square metres of office space from existing buildings in Civic, as well as renting 20,000 more in Capital Property Group's Constitution Place development.
Around 13,000 square metres of office space will be leased in Doma's Challis Street development on the site of the old Dickson Motor Registry.
"This combination of a new building and the occupation of existing office stock will provide an opportunity for developers and for existing building owners. It will also lead to the revitalisation of Civic and will result in positive outcomes for City businesses," Chief Minister Andrew Barr said at the time.
The strategy also involved the sale of ageing government office blocks like Macarthur House and 1 Moore Street, to cash in on the Commonwealth's asset recycling scheme.
However the government revealed last week it had reversed its decision to sell the Moore Street building after determining the sale would not be cost effective. The building will continue to be used by community health services and the CBR Innovation Network.
The ACT Property Council previously predicted there would be strong demand for office accommodation in Canberra in 2019, despite it being an election year.
Vacancy rates in Civic were 11 per cent in January, down from 13.2 per cent the previous year although higher than the Australia-wide rate of 8.5 per cent.