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Cusack received nominations for the Academy Award for Best Supporting Actress for her roles in the comedy-drama Working Girl (1988) and the romantic comedy In & Out (1997). Her other starring roles include those in Toys (1992), Addams Family Values (1993), Nine Months (1995), Cradle Will Rock (1999), Where the Heart Is (2000), Looney Tunes: Back in Action (2003), School of Rock (2003), and Kit Kittredge: An American Girl (2008). She has also provided the voice of Jessie in the Toy Story franchise (1999–present), for which she won an Annie Award, and Abby Mallard in Chicken Little (2005).

Cusack was a cast member on the comedy sketch show Saturday Night Live from 1985 to 1986. She starred on the Showtime hit drama comedy series Shameless (2011–2015) as Sheila Jackson, a role for which she received five consecutive Primetime Emmy Award nominations, winning for the first time in 2015. She is the sister of actress Ann Cusack and actor John Cusack.