Following her film debut in Acolytes (2008), she had a recurring role as Amanda Fowler on the television soap opera Neighbours (2009).

Heathcote has since appeared in several films, including In Time (2011), Pride and Prejudice and Zombies, The Neon Demon (both 2016), Fifty Shades Darker (2017), and Relic (2020).

[8][9] In February 2011, Tim Burton selected Heathcote to play Victoria Winters and Josette du Pres in his film adaptation of Dark Shadows, starring opposite Johnny Depp, Michelle Pfeiffer, and Helena Bonham Carter.

[17] She also joined the season 2 cast of television drama The Man in the High Castle as Nicole Dörmer, a Berlin-born filmmaker.

[21] Heathcote appears in the second season of the Australian web television series Bloom as a younger incarnation of Loris Webb, played by Anne Charleston.

The movie was produced by AGBO Films, the Russo Brothers' production company and Jake Gyllenhaal, and co-written and directed by Natalia Erika James.

[23] Heathcote stars with Toni Collette in the 2022 Netflix thriller series Pieces of Her, adapted from the Karin Slaughter novel of the same name.

[24] Heathcote stars in the Stan and Nine Network crime drama Scrublands as Mandy Bond, alongside Luke Arnold and Jay Ryan.

[28] She will also star alongside Teresa Palmer and Philippa Northeast in the television adaptation of Sally Hepworth's novel The Family Next Door for the ABC.