The ghosts of wartime Australia are still lingering in its fabric, but the Drill Hall Gallery is about to reopen as a fully repurposed landmark in Canberra's art scene.

The heritage-listed building on the edge of the Australian National University campus was built in 1940 to train soldiers for the 3rd Battalion Werriwa Regiment.

As with many buildings of the era, the spacious rooms and soaring ceilings turned out to be highly suited to displaying art, and the building was converted into an art gallery in 1984.

The ANU took over the building in 1992, with Nancy Sever as its inaugural director, and has steadily gained a reputation for diverse and high-quality exhibitions.

But it was never properly adapted to house art, and has been suffering from infrastructure problems and a famously dysfunctional air-conditioning system for decades.

Current director Terence Maloon said the building had been beset by decades of "bad interventions, quite an accumulation of them".

"We worked very hard to make it a lovely place to visit, but these lingering kinds of neglect and poor decision-making and so on and so forth made us feel a bit neglected," he said.

In response, the ANU committed more than $2 million to refurbishing the space, and the results are about to be unveiled.

Mr Maloon said the university had been "uncompromising" in its approach to the project, and the building was now thoroughly insulated with a state-of-the-art climate control system.

There's also a purpose-built curved-wall space to display one of the university collection's most popular works, Sidney Nolan's epic, nine-part masterpiece Riverbend.

"It's been a marvellous renovation with no shabby compromises, really," Mr Maloon said.

"Everything's been done well, thoughtfully, elegantly, the whole building looks cared for to the nth degree. It's a beautiful space and it really sings, and it has all the infrastructure of an excellent museum space."

The gallery itself also raised $160,000 for a new lighting system, enough to avoid the tender process and get "the best lighting that money could buy".

Mr Maloon said the response to the project in the art world showed the strength of Canberra's artistic landscape.

"We do something that I think is necessary and unique … that the state and national galleries in Australia no longer do," he said.

"We do thoughtful, rather large-scale surveys of very worthy contemporary artists. We're not a commercial gallery, we have a very strong relationship with the university and with the School of Art, but also with the art community."

He said the refurbished space would allow for smaller, more spontaneous displays, by local and emerging artists.

"That's working very well for us because that brings in younger people. We need that infusion," he said.

The gallery – complete with extended opening hours – is set to reopen on July 14 with an exhibition of works by a new generation of painters from the Western Desert epicentre of Papunya.

Streets of Papunya opens July 14 at Drill Hall Gallery and runs until August 14.