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Farmiga was encouraged to begin acting by her sister, and subsequently made her debut in her sister's film Higher Ground (2011). Thereafter, she rose to prominence for her work on the anthology series American Horror Story, starring in the seasons Murder House (2011), Coven (2013–2014), Roanoke (2016) and Apocalypse (2018). Her early film roles include the romantic comedy At Middleton (2013), the crime drama The Bling Ring (2013) and the psychological thriller Mindscape (2013), the latter of which was her first starring film role.

Farmiga was lauded for her performances in the comedy slasher film The Final Girls (2015), and the drama films 6 Years (2015) and Share (2015), all of which premiered at South by Southwest, which led her to be named one of the breakout stars of the festival. She has also provided the voice of Raven in the DC Animated Movie Universe (2016–2020), starred in the comedy films Rules Don't Apply (2016) and The Long Dumb Road (2018), the drama films In a Valley of Violence (2016) and What They Had (2018) and the supernatural thriller film The Nun (2018). Farmiga headlined the procedural drama series Wicked City (2015), and made her stage debut in the off-Broadway revival of the drama play Buried Child (2016).