She directed the films Radiance (1998), One Night the Moon (2001), Bran Nue Dae (2009), the courtroom drama telemovie Mabo (2012), and Jasper Jones (2017).

[8] Perkins' paternal grandmother's people were from Alice Springs, and she wanted to learn more about that side of the family's culture, so, after finishing school in 1988, she applied for a job as a television presenter with the Central Australian Aboriginal Media Association (CAAMA), mainly to get the airfare to fly there.

As she expected, she was not given the job, but they offered her a traineeship at Imparja Television, where she learnt the basics of production, including editing and sound recording.

[9][4] After starting her career as a filmmaker, in the early 1990s she won a scholarship to study production at the Australian Film, Television and Radio School (AFTRS) in Sydney, where she met and collaborated with Warwick Thornton.

[12] Perkins wrote, directed, and co-produced (with Ned Lander) a 55-minute documentary film about her father's 1965 protest bus journey into regional New South Wales, dubbed the "Freedom Ride".

She said later that it took a long time to cast the main characters, who included Trisha Morton-Thomas, Rachael Maza, and Deb Mailman, then a newcomer from Brisbane, and that they rehearsed for six weeks.

[9] In 2001 she co-wrote (with playwright John Romeril[18]) and directed the telemovie One Night the Moon, featuring musicians Paul Kelly, Kev Carmody, and Maireed Hannah.

[19] Bran Nue Dae, a film version of Jimmy Chi's 1990s hit stage musical, was directed by Perkins and released in 2009.

This tenth anniversary of the festival held at the Sydney Opera House featured the premiere of Fire Talker, a documentary film about her father Charlie Perkins by Australian filmmaker Ivan Sen.[20][21] Her courtroom drama / biopic telemovie about land rights campaigner Eddie Koiki Mabo, Mabo, featuring Jimi Bani and Deborah Mailman, was broadcast in 2012.

[22] Luke Buckmaster of The Guardian gave the film 4 out of 5 stars, praising its "superb cast" and saying "the series concludes at the peak of its power".

[23] Perkins executive produced the first series of First Contact (2014), a reality television show which challenged the non-Indigenous participants of Indigenous Australians.

[26] Perkins wrote, directed, presented, and produced the three-part documentary series The Australian Wars which aired on SBS and NITV in September 2022.

[10] Some of the many awards for which her films and TV productions have been nominated or won include: Perkins has a son with her ex-husband, filmmaker Richard McGrath.