Wolff's jazz pianist father Michael Wolff co-produced the series' soundtrack albums, The Naked Brothers Band (2007) and I Don't Want to Go to School (2008); the former of which ranked the 23rd spot on the Billboard 200 charts.

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He later became known for his lead role in the film Paper Towns (2015), and other films such as Admission, Behaving Badly, and Palo Alto, each of which premiered in 2013.

Wolff also co-starred in the highly successful theatrical film, The Fault in Our Stars (2014) before portraying Ed in the film Ashby in 2015.

He portrayed Dzhokhar Tsarnaev in Patriots Day (2016) and John "Derf" Backderf in My Friend Dahmer (2017).

Wolff began his acting career at the age of 6 in the 2005 musical comedy film The Naked Brothers Band: The Movie, written and directed by his mother.

He first gained recognition for starring alongside his older brother Nat in the Nickelodeon musical comedy television series The Naked Brothers Band (2007–09), which was created by the boys' mother Polly Draper.

Wolff and his brother released two soundtrack albums for the series, The Naked Brothers Band and I Don't Want to Go to School, which were co-produced by their father Michael Wolff.

In 2015, Wolff starred in Paper Towns, his second film adaptation of a John Green novel following The Fault in Our Stars.

He played the lead role, Quentin "Q" Jacobsen, a teenage boy in love with his neighbor (played Cara Delevingne).

He portrayed Light Turner in the Netflix adaptation of Death Note (2017).