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After graduating from high school, Sevigny found work as a model and appeared in music videos for Sonic Youth and The Lemonheads, which helped acquire her "it girl" status. In 1995, she made her film debut in Kids and became a prominent performer in the independent film scene throughout the late 1990s, with roles in such films as 1996's Trees Lounge. Sevigny rose to prominence with her portrayal of Lana Tisdel in the drama film Boys Don't Cry (1999), for which she received a nomination for the Academy Award For Best Supporting Actress.

Throughout the 2000s, Sevigny appeared in supporting parts in numerous independent films, including American Psycho (2000), Demonlover(2002), Party Monster and Dogville (both 2003), and The Brown Bunny (2004). Her participation in the latter caused considerable controversy due to a scene in which she performed graphic, unsimulated fellatio. From 2006 to 2011, Sevigny portrayed Nicolette Grant on the HBO series Big Love, for which she won a Golden Globe Award for Best Supporting Actress in 2010. She also appeared in mainstream films such as David Fincher's Zodiac (2007) and starred in numerous television projects, including the British series Hit & Miss (2012), and had supporting roles in Portlandia (2013), two seasons of American Horror Story; and in the Netflix series Bloodline (2015–2017) and Monsters: The Lyle and Erik Menendez Story (2024).

Sevigny made her directorial debut in 2016 with the short film Kitty. Her third film as a director, White Echo, competed for the Short Film Palme d'Or at the 2019 Cannes Film Festival. She also has a career in fashion design concurrent with her acting work. Over the years, her alternative fashion sense has earned her a reputation as a style icon.