Dourif starred as Bart Curlish in the BBC America science fiction series Dirk Gently's Holistic Detective Agency (2016–2017) , as Diane Jones in ABC miniseries When We Rise (2017), and Dr. Cassie McKay in the Max medical drama The Pitt (2025).

[3] In 2005, Dourif made her professional acting debut as Chez Ami Whore in the HBO period drama series Deadwood.

The same year, Dourif guest starred in the NBC police procedural series Law & Order: Special Victims Unit as Detective Nikki Breslin.

[6] In 2012, Dourif starred in the short film This is Caroline and appeared in Paul Thomas Anderson's psychological drama The Master.

[3] In 2014, she was cast in the indie films Gutshot Straight, Dangerous Words from the Fearless, Precious Mettle, and Fear Clinic.

[9] Also in 2017, she portrayed the younger version of the character played by Rachel Griffiths, named Diane Jones, in the ABC docudrama miniseries When We Rise.