Shawkat was born in Riverside, California. 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. She is of Iraqi heritage on her father's side and Irish-Norwegian on her mother's side.
Alia Shawkat made her film debut in the feature film Three Kings alongside George Clooney, playing Amir's daughter. From 2001 to 2002, Shawkat starred as Hannah Rayburn in the television sitcom State of Grace, aired in the United States on the cable television channel Fox Family (renamed ABC Family in 2001). She starred opposite Mae Whitman, who later appeared with Shawkat on Arrested Development. As Maeby Fünke, she was a regular cast member of the Fox Network series Arrested Development for the entire run of the show (2003–2006). On the Season 1 DVD, Alia remarks that her first kiss was an on-screen moment with Michael Cera, who played her cousin George Michael Bluth.
Shawkat has appeared in feature films. Her most recent role was playing an Arab-American teen in Cherien Dabis's film Amreeka. She has also appeared in Rebound, Three Kings, Deck the Halls, and Whip It.
She recently appeared in Har Mar Superstar's music video for Tall Boy.
Shawkat recently filmed The Runaways, a biographical movie on the band The Runaways. She stars as Robin, the band's fictional bassist.