Castle-Hughes is best known for her role as Paikea "Pai" Apirana in the movie "Whale Rider" (2002). For this she was was nominated for an Academy Award for Best Actress. She was the youngest person to be nominated for the award at the time. She has also appeared in the movies "" (2005), "Hey, Hey, It's Esther Blueburger" (2008) and "Red Dog" (2011). On television, she has appeared in "The Walking Dead", "Game of Thrones" and "".