Tunney made her film debut in the 1992 comedy Encino Man. She came to prominence with leading roles in the cult films Empire Records (1995) and The Craft (1996). She received the Volpi Cup for Best Actress, as well as Gotham and Independent Spirit nominations for her performance in Niagara, Niagara (1997). She had leading roles in the action-thriller films End of Days (1999), Supernova and Vertical Limit (both 2000). In 2006, she earned critical acclaim for her portrayal of a victim of sexual assault in the independent drama Open Window. Her other notable film appearances include Cherish, The Secret Lives of Dentists (both 2002), The In-Laws (2003), Hollywoodland (2006), August, The Burning Plain (both 2008), Passenger Side (2009), and Looking Glass (2018).