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Metcalf began her career with the Steppenwolf Theatre Company and frequently works in Chicago theatre. She made her Broadway debut in the 1985 play My Thing of Love. She went on to receive six Tony Award nominations, winning Best Actress in a Play in 2017 for her performance in A Doll's House, Part 2 and Best Featured Actress in a Play for the 2018 revival of Edward Albee's Three Tall Women. Her other Tony-nominated roles were for November (2008), The Other Place (2010), Misery (2016), and Hillary and Clinton (2019).

She gained national attention for her performance as Jackie Harris on the sitcom Roseanne (1988–1997, 2018) and its spinoff The Conners (2018–present), for which she won three Primetime Emmy Awards for Outstanding Supporting Actress in a Comedy Series. She also won a Primetime Emmy Award for her guest role in Hacks (2022), and her other Emmy-nominated roles include 3rd Rock from the Sun (1999), Monk (2006), Desperate Housewives (2007), The Big Bang Theory (2016), Getting On (2013–2015), and Horace and Pete (2016). She also appeared on The Norm Show (1999–2001), Frasier, and The Dropout (2022).

In film, Metcalf is best known for her performance as Marion McPherson in Greta Gerwig's comedy-drama film Lady Bird (2017). She was nominated for an Academy Award, a Golden Globe Award, a SAG Award, and a BAFTA Award. From 1995, she has voiced Mrs. Davis, the mother of Andy, in the Toy Story franchise, and voiced Sarah Hawkins in the Disney animated Treasure Planet (2002). Other notable film credits include Desperately Seeking Susan (1985), Uncle Buck (1989), JFK (1991), Dear God (1996), Georgia Rule (2007) and Scream 2 (1997).