Powley played the lead role of Minnie Goetze in the comedy-drama film The Diary of a Teenage Girl, which premiered in New York City and Los Angeles in August 2015.

Shortly afterward, Powley starred as the titular character in the 2016 indie film Carrie Pilby, taking over the role from Hailee Steinfeld.

[10] In June 2020, Powley appeared in The King of Staten Island as the love interest of Pete Davidson's character.

[16] She appeared as Dawn in the March 2018 revival of Lobby Hero at the Hayes Theatre, alongside Chris Evans, Michael Cera and Bryan Tyree Henry.

[18] It was announced in July 2021 via actor Douglas Booth's Instagram page that he and Powley were engaged to be married, having met on the set of the film Mary Shelley in 2016.

The couple were married under a chuppah made by Booth's sister, an artist, to honour Powley's Jewish heritage.