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Following a series of minor credits, Campbell had a starring role in the drama series Catwalk (1992–1993) and the television film The Canterville Ghost (1996). She subsequently relocated to the United States to star as Julia Salinger in the Fox teen drama series Party of Five (1994–2000), which became her breakthrough role. She rose to international prominence for her leading role as Sidney Prescott in Wes Craven's slasher film Scream (1996), which spawned the Scream franchise, in which she reprised her role in each film except the sixth. She also headlined the horror film The Craft (1996), the thriller film Wild Things (1998), and the drama film Panic (2000).

Campbell starred in, produced, and wrote the story for Robert Altman's drama film The Company (2003). After a hiatus, she returned to television with a recurring role on the drama series Medium (2007) and starring roles on the action series The Philanthropist (2009) and the miniseries Titanic: Blood and Steel (2012). She appeared in the action film Skyscraper (2018). The drama film Clouds (2020), and had starring roles on the political thriller series House of Cards (2016–2017) and the crime drama series The Lincoln Lawyer (2022–present).