She is known for her performances as Maeby Fünke in the Fox/Netflix television sitcom Arrested Development (2003–2006; 2013–2019), Dory Sief in the TBS and HBO Max dark comedy series Search Party (2016–2022), and Gertie Michaels in the 2015 horror-comedy film The Final Girls, as well as her roles in State of Grace and The Old Man.

"[12] 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.

[12] According to The Hollywood Reporter, the show "follows two painfully cool hipsters as they relocate from Brooklyn's Williamsburg neighborhood to Los Angeles' Silver Lake enclave in hopes of becoming artists—of any kind.

"[13] Shawkat, along with State of Grace and Arrested Development co-star and close friend Mae Whitman, sang guest vocals on several tracks from indie-punk band Fake Problems' 2010 album Real Ghosts Caught on Tape.

[14] Six years after the series was canceled by Fox, filming for a revived fourth season of Arrested Development began on August 7, 2012, and Shawkat reprised her role as Maeby Fünke.

[16] In 2015, Shawkat guest-starred on Broad City, portraying the romantic interest and look-alike of Ilana Glazer's character for one episode; the two were attracted to one another due only to their similar appearances.

[17] Shawkat starred in the lead role of Dory Sief on the TBS comedy Search Party, which premiered on November 21, 2016[18] and moved to HBO Max in 2019 before concluding with its fifth and final season in January 2022.