Lerman played the lead, Marcus Messner, in Indignation, an adaptation of Philip Roth's 2008 novel of the same name, directed by James Schamus; his character is a student who faces antisemitism and sexual repression while coming of age at a 1950s Ohio college. Indignation premiered at the 2016 Sundance Film Festival, and was theatrically released in July 2016.
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Lerman received positive reviews for his work, and was again nominated for the Young Artist Award - Best Performance in a Feature Film - Leading Young Actor (2008).
It was the second consecutive year he received a nomination in that category, although this time he did not win.
He made his film debut in 2000's The Patriot, playing William Martin, one of the children of Mel Gibson's character.
The same year, he appeared in another Mel Gibson film, What Women Want, playing Gibson's character as a child.
stated that, though the film was uneven, Lerman "displays a supreme confidence". Also that year, Lerman had a leading role in the Renée Zellweger comedy feature My One and Only, playing a teenage character based on actor George Hamilton – depicted as an aspiring writer who, after his parents split, accompanies his mother and brother on a cross-country trip, eventually arriving in Hollywood.