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She began her acting career appearing in television programs throughout the 1980s. In 1986, she appeared in her first film role, with her breakthrough coming in the 1990 Coen brothers-directed Miller's Crossing.

Her next notable film credits include The First Wives Club (1996), Flubber (1997), and Space Cowboys (2000). She received an Academy Award for Best Supporting Actress for her role as Lee Krasner in Pollock (2000). She had a supporting role in Mona Lisa Smile (2003). She received a second Academy Award nomination for her performance as Celeste Boyle in the drama film Mystic River (2003).

She appeared in several 2007 films, including Sean Penn's Into the Wild and Frank Darabont's The Mist, based on the novella by Stephen King. Also in 2007, she shared top billing with Kevin Bacon in Rails & Ties, the directorial debut of Alison Eastwood. Harden played a woman who has a mastectomy in Home (2008). (Her character in Rails & Ties also had a mastectomy.) One scene required her to bare her breasts, with the missing breast removed using computer-generated imagery. In Home, her co-stars include her daughter, Eulala Scheel.

In 2009, she had quite a busy year. She appeared as a regular on the FX series Damages as a shrewd corporate attorney opposite Glenn Close and William Hurt. She co-starred in the films Whip It, and The Maiden Heist. She returned to Broadway in Yasmina Reza's God of Carnage, co-starring with James Gandolfini, Hope Davis and Jeff Daniels. All three actors were nominated for a Tony Award; Harden won Best Actress in a Play. She received her first Primetime Emmy Award nomination for her role as FBI Special Agent Dana Lewis in the crime drama series Law & Order: Special Victims Unit, and earned a second Primetime Emmy Award nomination for her performance as Janina Krzyżanowska in the television film The Courageous Heart of Irena Sendler (2009).

She reunited with her former Broadway co-star Jeff Daniels as a new cast member on HBO's series The Newsroom in 2013. In 2015, she had a starring role in the medical drama Code Black. Her other notable television credits include ABC's How to Get Away with Murder and the Apple TV+ series The Morning Show.

She played Christian Grey's mother, Grace Trevelyan Grey, in the Fifty Shades film series from 2015 to 2018. She stars in the 2022 CBS drama So Help Me Todd.