Since she made her film debut, Castle-Hughes has appeared in various films including Hey, Hey, It's Esther Blueburger (2008), New Zealand tele-movie Piece of my Heart (2009) and a small role in Star Wars Episode III: Revenge of the Sith (2005). She played the main role of the Virgin Mary, in the film The Nativity Story in (2006). She also appeared in Red Dog (2011) and Thank You for Your Service (2017), among others.
She is known for her role as Obara Sand on Game of Thrones and her main role as Special Agent Hana Gibson on FBI: Most Wanted. She also had recurring roles on Roadies (2016), Manhunt (2017), and On the Ropes (2018).