In 2005, Castle-Hughes had a small part as Queen Apailana in Star Wars: Episode III – Revenge of the Sith. In 2006, she portrayed the starring role of the Virgin Mary in The Nativity Story. New York Times critic, A. O. Scott, said that she "seemed entirely unfazed by the demands of playing Mary. She had the poise and intelligence to play the character not as an icon of maternity, but rather as a headstrong, thoughtful adolescent transformed by an unimaginable responsibility." The Christian-themed film earned only $8 million during its opening week, but its box office surged during the week of Christmas,.

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