Popplewell, eldest of three children, is the daughter of Andrew Popplewell and Dr. Debra Lomas, a dermatologist. She was born in London. She has two younger actor siblings: Lulu Popplewell, who starred as Daisy in Love Actually, and Freddie Popplewell, who starred as Michael Darling in the film Peter Pan. Her paternal grandfather, Sir Oliver Popplewell, is a distinguished former judge. She attended North London Collegiate School and was senior student 2006-2007. She was admitted to the University of Oxford in July 2007 and began a career in English and English Literature in September of the same year. She earned her degree in September 2010.
Popplewell began acting at the age of six, taking classes at the Allsorts Drama School. She began acting professionally in the TV production Frenchman's Creek in 1998. She made her film debut in 1999 in the film Mansfield Park and has since appeared in supporting roles in films like The Little Vampire (2000) and Girl with a Pearl Earring (2003) with Scarlett Johansson. In 2001, she appeared as Victoria in the BBC serial Love in a Cold Climate. Her first major role was in the film The Chronicles of Narnia: The Lion, the Witch and the Wardrobe (2005), where she played Susan Pevensie. She has a phobia of mice, which required a double to do part of her scene at the Stone Table in The Lion, the Witch, and the Wardrobe. She reprised her role in the sequel, The Chronicles of Narnia: Prince Caspian, in which she acted with William Moseley, Skandar Keynes, Georgie Henley, and Ben Barnes. The film opened in cinemas 16 May 2008. She also made a cameo appearance in the third Narnia film, The Chronicles of Narnia: The Voyage of the Dawn Treader, despite her character's absence in the book on which it is based. She was awarded the Cuppers Prize in 2007 for Best Supporting Actress in a student production of Five Kinds of Silence. In December 2007, she played Lady Macbeth in a student production of Macbeth at the OFS Studio in Oxford. In 2008, she performed as the character Wendla in the controversial play Spring Awakening. In 2012, she played the character Chyler Silva in the live action five-part miniseries Halo 4: Forward Unto Dawn. In March 2013, it was announced that Popplewell would star in the CW Television Network's pilot Reign. She portrayed Lola, one of the ladies-in-waiting and best friends of Mary, Queen of Scots. Filming took place in Ireland and Toronto, Canada.
The Little Vampire
Me Without You
Girl with a Pearl Earring
The Chronicles of Narnia: The Lion, the Witch and the Wardrobe
The Chronicles of Narnia: Prince Caspian
The Chronicles of Narnia: The Voyage of the Dawn Treader