She won a Genie Award in 1997 as Best Actress in a Leading Role for Kissed, was nominated for an Independent Spirit Award as best female lead in 2001 for her role in The Center of the World, and has twice been nominated for a Genie Award as best supporting actress she won in 2002 for Last Wedding.
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Parker is known for taking on controversial roles, such as her performance in Kissed, her role as a sympathetic lap dancer and paid escort in The Center of the World 2001 , and a rabbi in Six Feet Under.
She co-starred in Josephine Decker's 2018 feature film, Madeline's Madeline.
In 2014, she appeared as Congresswoman Jacqueline Sharp in the second season of the Netflix series House of Cards.
In 2012, Parker joined the cast of the television series The Firm, based on John Grisham's eponymous 1991 novel and its 1993 film adaptation; she portrayed Abby McDeere, wife of Mitch McDeere portrayed by Josh Lucas.