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She began to appear in supporting roles in films during the mid-1980s like box office hit Top Gun, achieving recognition in independent films such as Promised Land (1987) before her performance in the Rob Reiner-directed romantic comedy When Harry Met Sally... (1989) brought her widespread attention and her first Golden Globe nomination.

She subsequently established herself, both nationally and internationally, as one of the most successful actresses in the 1990s and early 2000s, particularly in romantic comedy films such as When Harry Met Sally (1989), Joe Versus the Volcano (1990), Prelude to a Kiss (1992), Sleepless in Seattle (1993), French Kiss (1995), You've Got Mail (1998), and Kate & Leopold (2001). Her other films include Top Gun (1986), Innerspace (1987),  The Doors (1991), Anastasia (1997), When a Man Loves a Woman (1994), Courage Under Fire (1996), Addicted to Love (1997), City of Angels (1998), Proof of Life (2000), Against the Ropes (2004), and The Women (2008). In 2015, she made her directorial debut with Ithaca, in which she also starred.

In 1995, critic Richard Corliss called her "the current soul of romantic comedy." Multiple film critics and media outlets have cited her as one of the best actors never to have received an Academy Award nomination.

She was married to actor Dennis Quaid (1991-2001), and they have a son, Jack. In 2000, she became romantically involved with actor Russell Crowe while working on their film Proof of Life. In January 2006, she adopted a 14-month-old girl from China whom she named Daisy True. She was in a relationship with American singer-songwriter John Mellencamp (2010-2014). They reunited in 2017, and announced their engagement on November 8, 2018. In October 2019, it was reported that she had ended their engagement.