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In 1999, she won the Primetime Emmy Award for Outstanding Supporting Actress in a Drama Series for her work on The Practice, and she was awarded the Women in Film Lucy Award. In 2005, she earned Golden Globe and Emmy nominations for her work in the miniseries Elvis.

Her breakthrough was her one-woman show "Wake Up, I'm Fat", which played off-Broadway at Classic Stage Company in 1994. She adapted the show into a book of the same name, which was published by Broadway Books in 1999.

She worked for a while as a sign language interpreter at hospitals. Her knowledge of sign language was used on The Practice, in an episode of Law & Order, and in her role as a child behavioral psychologist in the movie Mercury Rising.

In 2015, Manheim was in the Deaf West production of the musical Spring Awakening as Adult Women. The production, which had a cast composed half of hearing actors and half of deaf or hard-of-hearing actors, paired every deaf actor (who signed their lines in American Sign Language) with a hearing actor who said their lines verbally. Manheim voiced for deaf actress Marlee Matlin as well as signing her own dialogue in the parts of Frau Bergmann, Fräulein Großebüstenhalter, and Fräulein Knuppeldick.

Her other television credits include Chicago Hope, Ally McBeal, Family Guy, Will & Grace, Boston Public, Two and a Half Men, The L Word, How I Met Your Mother, and Hannah Montana. Since 2022, she has been part of the main cast of the revival of Law & Order.

Her film credits include Romy and Michele's High School Reunion, The Laramie Project, Scary Movie 3, Dark Water, and An Unfinished Life.

In August 2019, she was elected secretary-treasurer of the SAG-AFTRA union. Manheim was elected to the secretary-treasurer position. She did not run for reelection in 2021, and was succeeded by Joely Fisher.