Pirrie's professional acting career began in 2009. She made her debut at the Royal National Theatre in a 2010 production of Men Should Weep alongside numerous other Scottish actors. Shortly afterwards, she appeared in Solstice, a short film released in 2010. Her first role in a feature film was in Shell (2012), a Scottish drama in which Pirrie played the eponymous main character. For this performance she won Most Promising Newcomer at the British Independent Film Awards 2013 and was nominated for Best British Newcomer at the 2012 BFI London Film Festival Awards. In 2013, she played a Politician in "The Waldo Moment", an episode of the anthology series Black Mirror. In the same year she was named as one of BAFTA's "Breakthrough Brits" and Screen International's "UK Stars of Tomorrow".
In 2014, Pirrie starred in the BBC miniseries The Game, a Cold War spy thriller in which she played an MI5 secretary. The following year she appeared as Sheila Birling in Helen Edmundson's BBC One adaptation of J. B. Priestley's An Inspector Calls, in the miniseries The Last Panthers, the British independent film Burn Burn Burn, and the Italian film Youth.
In 2015, she starred as Ellie in the Academy Award winner for Best Live Action Short Film, Stutterer. Ellie is the love interest for Greenwood (played by Matthew Needham). Greenwood has a major stuttering Problem and can't speak effectively, causing him to panic when Ellie suggests they take what had only been an online relationship, offline to meet in person. After finally giving in, Greenwood learns a secret about Ellie that changes everything.
She also plays Lara in the 2016 BBC thriller series, The Living and the Dead. In 2017, she starred in the Netflix series, The Crown for its second season, playing Eileen Parker. In 2018, she appeared in the BBC/Netflix miniseries Troy: Fall of a City.
