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Foy was educated at Aylesbury High School from the age of 12 and later attended Liverpool John Moores University, studying drama and screen studies. She also trained in a one-year course at the Oxford School of Drama. She graduated in 2007 and moved to London's Peckham district to share a house with five friends from drama school. While at the Oxford School of Drama, Foy appeared in the plays Top Girls, Watership Down, Easy Virtue, and Touched. After appearing on television, she made her professional stage debut in DNA and The Miracle, two of a trio of single acts directed by Paul Miller at the Royal National Theatre in London (the third was Baby Girl).

Foy gained international recognition for portraying the young Queen Elizabeth II in the first two seasons of the Netflix series The Crown, for which she won a Golden Globe and a Primetime Emmy, among other awards. In 2018, she starred in Steven Soderbergh's psychological thriller Unsane and portrayed Janet Shearon, wife of astronaut Neil Armstrong, in Damien Chazelle's biopic First Man. For the latter role, she was nominated for a BAFTA and a Golden Globe.