She made her acting debut in the drama film Whale Rider (2002), for which she was nominated for the Academy Award for Best Actress, making her the second-youngest nominee in such category.

Castle-Hughes was born in 1990 in Donnybrook, Western Australia to a Māori mother, Desrae Hughes, of Ngāti Porou, Tainui, and Ngāpuhi descent,[1] and Tim Castle, an Anglo-Australian father.

[1] In 2002, Castle-Hughes made her debut in the film Whale Rider, in which she played the main role of Paikea Apirana (Pai).

She had no previous acting experience and went directly from her Auckland school classroom to the film set when the shoot began in New Zealand in late 2001.

[8] Castle-Hughes reunited with New Zealand director Niki Caro for the film adaption of The Vintner's Luck, which had its international premiere in September 2009.

Castle-Hughes starred in the Japanese horror film Vampire,[9] and she also played a recurring role as Axl's flatmate in The Almighty Johnsons which premiered in 2011.

In 2011 Castle-Hughes also played a minor part in the film Red Dog as Rosa the veterinary assistant and wife of Vanno.

[12] Castle-Hughes found out that she had won the role the night the Season 4 episode "The Mountain and the Viper" aired, in which her on-screen father's death was shown.

New Zealand Prime Minister John Key initially admonished her to "stick to acting", but offered a week later to discuss the issues with her over tea after she maintained she knew more about them than he gave her credit for.