Shawkat was born in Riverside, California, to actor Tony Shawkat, and Dina Burke; she has two brothers. She grew up in nearby Palm Springs.

Shawkat is of Iraqi Kurdish descent on her father's side and Irish and Norwegian descent on her mother's side. Her maternal grandfather was actor Paul Burke (1926–2009), who appeared as Detective Adam Flint on the TV series Naked City (1959–1963) and as Lyon Burke in the 1967 movie Valley of the Dolls.

Shawkat made her acting debut in both film and television in 1999. In that year, she played the daughter of the character Amir in the feature film Three Kings, in which her father Tony Shawkat played a member of the Iraqi Republican Guard, and appeared as a young Sarah "Mac" MacKenzie on one episode of JAG. She landed her first starring role in 2001, playing Hannah Rayburn in the television sitcom State of Grace, which aired in the United States on the cable television channel Fox Family (subsequently renamed ABC Family) until 2002. She later played Maeby Funke on Arrested Development.

As Maeby Fünke, Shawkat was a regular cast member of Arrested Development for the entire run of the show (2003–2006). The series received nearly universal positive reviews, with Shawkat's performance occasionally singled out for praise; pop-culture commentator Brian M. Palmer remarked that she was "one of the brightest lights on a show populated solely by bright lights," and Scott Weinberg of eFilmCritic described her as "one funny young lady." In an interview with The A.V. Club in 2010, Shawkat remarked that many of her "formative moments" as an actress took place on the Arrested Development set: " [Show creator] Mitch Hurwitz was like a father figure to me...In a way, it was great to be around [the cast], because I feel that my understanding of comedy was able to grow really well during that time."

Since the end of Arrested Development, Shawkat has continued to act in feature films. In 2010, she appeared in The Runaways, a biographical movie about the band of the same name, playing a fictional version of the band's bassist. In 2009, she played an Arab-American teen in Cherien Dabis's film Amreeka and appeared in Drew Barrymore's directorial debut Whip It alongside Ellen Page. She has also appeared in the films Rebound, Deck the Halls, Prom Wars, and Bart Got a Room.

In 2009, Shawkat appeared in Whip It co-star Har Mar Superstar's music video for "Tall Boy", which also featured Eva Mendes and Eric Wareheim. In October 2009, it was announced that Shawkat, Har Mar, and fellow Whip It co-star Page would produce and write a show for HBO called Stitch N' Bitch. According to the Hollywood Reporter, the show "follows two painfully cool hipster girls as they relocate from Brooklyn's Williamsburg neighborhood to Los Angeles' Silver Lake enclave in hopes of becoming artists – of any kind."