An exhibition celebrating the brilliance of Aboriginal and Torres Strait Islander art will headline the long-awaited re-opening of the Potter Museum of Art (The Potter) in Naarm next year.

65,000 Years: A Short History of Australian Art will investigate the dark heart of the nation's art history, and will be curated by Professor Marcia Langton, Associate Provost Judith Ryan and Shanysa McConville, in consultation with Indigenous custodians.

"The ironic title of this exhibition refers to the belated and reluctant acceptance of Aboriginal and Torres Strait Islander art into the fine art canon by Australian curators, collectors, art critics and historians in the last quarter of the 20th Century," Professor Langton said.

"65,000 Years: A Short History of Australian Art celebrates Indigenous art as it is increasingly recognised in galleries and collections around the world - as the greatest single revolution in Australian art."

The exhibition will feature seven major new artist commissions by leading contemporary Indigenous artists and will examine the rise in prominence and popularity of Indigenous art in Australia, as well as the important cultural and design traditions, knowledge, and agency.

Overall, the exhibit will feature more than 400 artworks as part of a year-long program to mark the return of patrons to the University of Melbourne's flagship art museum.

Director of Art Museums, Charlotte Day, said The Potter was uniquely positioned to hold such an exhibition at an "important time in Australia's history".

"Since 1853, the University has collected works of art, cultural objects and records that form a profoundly important archive, and for the first time these Indigenous collections will be exhibited together and interpreted by authoritative Indigenous scholars and other leading experts," Ms Day said.

Alongside the exhibit, a new education initiative will take place, creating resources to help build a deeper understanding of First Nations art, history, and culture for primary and tertiary students, which will continue to be available after the exhibit ends.

Developed in partnership with the University's Ngarrngga Project, which builds innovating curriculum resources in collaboration with Indigenous knowledge experts and is led by Associate Dean (Indigenous) in the Faculty of Education, Professor Melitta Hogarth, in conjunction with Professor Langton; Director of the Indigenous Knowledge Institute, Professor Aaron Corn; and Dean of the Faculty of Education, Professor Jim Watterston.

The university has been forced to confront its controversial past with the release of a new book, "Dhoombak Goobgoowana: A History of Indigenous Australia and the University of Melbourne."

The 500-page examination of the institution reveals a history of Nazi apologists, antisemites, racists, and eugenicists - all on the faculty. Some of these men, until very recently, even had buildings and scholarships named after them.

Vice-Chancellor, Professor Duncan Maskell, said alongside the book, the exhibit and program was an important exercise in truth-telling for the university.

"It will provide a vital platform for Indigenous storytelling and encourage dialogue about the importance of Indigenous culture, history and art," Professor Maskell said.

A comprehensive publication to accompany the exhibit will be released by Thames & Hudson on September 24 this year, edited by Judith Ryan and Professor Langton.

It will feature new writing by 25 thinkers across a variety of disciplines and generations, further examining the significant body of artwork in the exhibition across media, time periods, regions, and language groups.

More information on the program will be announced later this year.