She gained further notice for her role as a Las Vegas escort in the drama The Center of the World (2001), for which she was nominated for the Independent Spirit Award for Best Female Lead.

In 2011, she appeared as a recurring guest star in the sixth season of Dexter, before being cast as politician Jacqueline Sharp on the Netflix series House of Cards in 2014.

She played the daughter of Margarethe Cammermeyer, a lesbian military officer, in the television film Serving in Silence (1995), opposite Glenn Close and Judy Davis.

[5] She also appeared in a minor role as a nurse in the Western Last of the Dogmen (1995),[9] as well as the Lifetime holiday television film Ebbie (also 1995) playing the niece (and sister) of Susan Lucci's Scrooge character, in a modern retelling of Charles Dickens's A Christmas Carol.

[5] Also in 1996, Parker appeared in an episode of the Canadian horror series Poltergeist: The Legacy, as well as Bruce McDonald's independent film Hard Core Logo, in which she portrayed an aspiring actress.

[15] She subsequently appeared as a pregnant woman in Michael Winterbottom's Wonderland (1999), and in the historical drama Sunshine (also 1999), playing a Hungarian Jew during World War II.

[16] Parker's first major American film was the drama Waking the Dead (2000), in which she co-starred with Billy Crudup and Jennifer Connelly, playing the socialite girlfriend of a political candidate.

The same year, Parker appeared in the low-budget independent film The Center of the World, directed by Wayne Wang, in which she starred as a stripper who accompanies a man (played by Peter Sarsgaard) on a weekend in Las Vegas for $10,000.

[5] The same year, she had a supporting role in the thriller Max, starring John Cusack and Noah Taylor,[19] and also guest-starred in two episodes of the HBO series Six Feet Under, playing a rabbi.

[22] Derek Elley of Variety praised the performances, writing: "Slater and Parker make a sharp pair of leads, each handling their dialogue with crisp efficiency.

"[22] The same year, she starred in the historical drama Iron Jawed Angels, opposite Hilary Swank and Frances O'Connor, which charts the lives of several suffragists, including Alice Paul and Lucy Burns.

The following year, she guest-starred in one episode of Party Down,[29] and subsequently appeared in a supporting role in the post-apocalyptic thriller The Road, playing a woman trying to survive after an apocalyptic event.

[20] In 2010, Parker starred in the Canadian police procedural Shattered, which also aired for a single season, and had a lead role in the independent drama Trigger, opposite Tracy Wright, in her final film appearance before her death.

[34] Parker was subsequently cast alongside Jamie Dornan, Sarah Gadon, and Aaron Paul in the supernatural thriller The 9th Life of Louis Drax (2016), directed by Alexandre Aja.