Milioti's first acting roles were bit parts in national advertising campaign ads, notably one for the Ford Edge. She appeared in television programs such as The Sopranos and films such as Greetings from the Shore. Milioti appeared in stage performances. In 2007, she appeared on Broadway as Alice Ashbrook in Helen Edmundson's award-winning adaptation of Jamila Gavin's novel Coram Boy. In 2010, she starred in That Face, and was nominated for a Lucille Lortel Award for Outstanding Lead Actress for her work in Stunning.
In 2012, she received a Tony Award nomination for Best Actress in a Musical for her portrayal of Girl in Once, a musical in which she performed from 2011 to 2013. Of her performance, Ben Brantley of the New York Times wrote: "It's not easy playing a winsome life force with a foreign accent. But Ms. Milioti has mastered the assignment brilliantly. She brings a new confidence to her portrayal, and an enhanced mixture of wit and wisdom, which suggests a maturity in youth, a fatalism hard won during an Eastern European childhood. And together she and Mr. Kazee exude a chemistry that is all the more achingly real for being so subdued." Her Once performance, with fellow principal soloist Steve Kazee, earned the 2013 Grammy Award for Best Musical Theater Album. She also read aloud a short story for the 2011 This American Life episode "Adventure". In 2012, she appeared on several songs of Glen Hansard's debut album Rhythm and Repose.
In 2013, Milioti was cast in the CBS sitcom How I Met Your Mother as the titular Mother, appearing for the first time in the season eight finale titled "Something New", and was promoted to a series regular for the show's ninth and final season. Milioti portrayed Jordan Belfort's first wife, Teresa Petrillo, in the 2013 Martin Scorsese film The Wolf of Wall Street. In February 2014, she was cast as Zelda, the female lead on NBC's comedy A to Z which premiered that October and aired for one season of 13 episodes. In 2015, she co-starred on the second season of FX's Fargo as Betsy Solverson, the cancer-stricken wife of state trooper Lou Solverson and mother of future deputy Molly Solverson. In 2017, Milioti appeared in the fourth season of the sci-fi anthology show Black Mirror in the episode "USS Callister" as Nanette Cole, a newly employed game developer whose digital recreation becomes trapped in a virtual simulator game.
In 2020, Milioti starred in the sci-fi/comedy Palm Springs, which premiered at the Sundance Film Festival in January and on Hulu in July. In 2021, she starred in the HBO Max dark comedy series Made for Love as the entrapped wife of a tech billionaire from whom she runs away.
In 2024, Milioti starred as Sofia Falcone in the HBO spin-off miniseries of The Batman titled The Penguin, opposite Colin Farrell. Her performance earned her a nomination for the Golden Globe Award for Best Actress – Miniseries or Television Film.
Cristin Milioti, After the Blast
Cristin Milioti, Once
Cristin Milioti, Once
Cristin Milioti, Once
Cristin Milioti, Once
Cristin Milioti, Stunning
Cristin Milioti has appeared on Broadway in 3 shows.
Cristin Milioti has not appeared in the West End.
Outstanding Lead Actress in a Play (The Lortels) for After the Blast, Distinguished Performance Award (Drama League Awards) for Once, Outstanding Actress in a Musical (Outer Critics Circle Awards) for Once, Outstanding Lead Actress (The Lortels) for Once, Best Performance by an Actress in a Leading Role in a Musical (Tony Awards) for Once and Outstanding Lead Actress (The Lortels) for Stunning.
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