Hunter is a descendent of the Nunukul people of the Munaldjali clan of the Yagambeh tribe.

Born in Sydney in 1993 to Cynthia Lochard, formerly of New York City Ballet, and Bangarra’s Artistic Director Stephen Page, Hunter is a descendent of the Nunukul people of the Munaldjali clan of the Yagambeh tribe. Hunter has appeared on stage in Bangarra's Blak (2013), Boomerang (2005), Skin (2000) and Praying Mantis Dreaming (1993), and Stephen Page’s Kin and Bloodland for the Sydney Theatre Company and Adelaide Festival.

In 2015 Hunter attended the Toronto International Film Festival for Stephen Page's feature film debut Spear (2015), in which Hunter played the lead, Djali. Hunter released his debut short film Djali at the Sydney Film Festival, which he wrote, directed, produced, edited. The film went on to play at Cinefest Oz, Flickrfest and St Kilda Film Festival, where Hunter was nominated for Best Actor for his performance.

Hunter has also appeared in various films and TV series including Les Norton, Tidelands, Bran Nue Dae, The Saphires, Around the Block, Wentworth, Soul Mates, Water Rats, East West 101, Shadow Trackers, and Harrow, and wrote and presented a NAIDOC Week episode for ABC’s Play School, titled Acknowledgement of Country. He also played the lead role in the critically acclaimed show Cleverman, for which Hunter received a nomination for the Graham Kennedy Award for Most Outstanding Newcomer at the Logie Awards.

Hunter has also featured in several short films including Adrian Wills' Arcadia and Wayne Blair's Black Talk and The Djarn Djarns, which won the Crystal Bear for Best Short Film at the 2005 Berlin International Film Festival.