The Gallery collects Aboriginal and Torres Strait Islander art and artefacts to demonstrate the geographic and cultural diversity of Indigenous Australians. The Fine Gallery of contemporary Aboriginal art is one of the most significant in an Australian regional gallery. The collection focuses on West Arnhem Land and the Central Desert with the development of the Papunya School. There are also works from the Tiwi people of Bathurst and Melville Islands, situated off the far North Coast of Australia, and a significant collection of contemporary works by Illawarra and South Coast Aboriginal artists. The collection showcases the diversity of styles which exist between different Aboriginal groups and between individual artists.

The Aboriginal collection features objects including carved wood, and stone male and female busts by John Gilbert from the Kimberley region, Western Australia, Didgeridoo and sculpture from local artists Jeff Timbery and Laddie Timbery, and two Tiwi Pukumani poles from Bathurst Island, Northern Territory. The collection also includes a large representation of barks form Eastern and West Arnhem land.

Aboriginal paintings on canvas include works by: Robert Ambrose Cole, Abie Jungala, Emily Kame Kngwarreye, Mary Mclean, Jean Nampajinpa, Linda Syddick Napaltjarri, Mary Dixon Nungarrayi, Gloria Tamerre Petyarre, Prince Of Wales, Wenten Rubuntja, William Sandy, Rover Thomas, Freddie Timms, Long Jack Phillipus Tjakamarra, Maxie Tjampitjimpa, Billy Stockman Tjapaltjarri, Clifford Possum Tjapaltjarri, Barney Daniels Tjungurrayi, Charlie Tjaruru Tjungurrayi, Colin Dixon Tjungurrayi, Gideon Tjupurrula, Judy Watson, Judy Napangardi Watson, Harry Wedge and Lucy Yukenbarri.