"You could be forgiven for thinking it's just a collection of tapestries and portraits of prime ministers," the manager of the Parliament House art collection, Justine van Mourik, says of most people's experience of the 6000-piece collection.

Ms van Mourik describes is as an "unusual" and "eclectic" collection "with an historical bent."

"[People] might be surprised by the breadth and depth of what's on show. All of these things tell different stories and different facts about what it means to be Australian. It reflects Australia's cultural life and society."

About 2000 works are in storage at any given time and the rest hang on the walls of Parliament House, Admiralty House, Government House or are on loan to other galleries.

Although Parliament House has a significant art collection it was not designed with the display of art in mind.

The abundance of natural light is not kind to works of art, particularly paintings, and they are regularly rotated to conserve them.

Works not on display are housed in a secure subterranean storage room, photographed for the first time for this story, with its own security code and its own climate.

About 50 new pieces are acquired for the collection each year.

"Every now and then you see something and think 'I just have to have it'," Ms van Mourik says.

The competitive nature of the art world places her at a disadvantage, bound as she is by the collection's rules of acquisition.

A list of pieces she would like to buy is discussed twice a year by the committee in charge of approving new works. It is made up of Ms van Mourik, an advisor from the National Gallery of Australia and the presiding officers, the Speaker of the House of Representatives, Bronwyn Bishop, and the President of the Senate, Stephen Parry, and their deputies.

"Madam Speaker [Bronwyn Bishop] has a very good eye," Ms van Mourik says.

"She really knows what works spatially."

Many of the works on display are in the offices of politicians and are allocated depending on seniority and the size of one's office.

The basic standard for a backbencher is four works for the walls and one decorative piece.

"Indigenous art is always really popular," Ms van Mourik says. "Some like to represent their areas. If they're from Queensland, they like something from Queensland."

On the walls of Prime Minister Tony Abbott's offices hang a portrait of the Queen and a black and white portrait of Robert Menzies by Louis Kahan.

In Opposition leader Bill Shorten's suite are works by Tim Storrier, Grace Cossington Smith and Clifton Pugh.

The problem of the accessibility of the collection will be partially addressed, Ms van Mourik hopes, by digitising it and making it available on the internet.

Two public tours, including a trip to the underground storage room, will also be offered to the public late in February as part of Canberra's Enlighten festival.

Ms van Mourik also oversees the painting of new portraits.

Every prime minister, governor general and presiding officer has a portrait painted of them once they leave office (as does the head of state but that has not been an issue for decades thanks to the longevity of Her Majesty, Queen Elizabeth II).

Subjects are able to choose the artist who will depict them with help from the National Portrait Gallery of Australia and Ms van Mourik.

The only former prime minister to buck the system was Gough Whitlam whose portrait had already been painted by Clifton Pugh while he was in office.

"He insisted that was purchased not commissioned," Ms van Mourik says. "He just felt no one else could do a better job and that would be the way he wanted to be represented."