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In 2004, he made his directorial debut with the short film Let's Love Hate and later directed a short film titled Maniac (2011), starring American rappers Cage and Kid Cudi.

In 2007, LaBeouf starred in the commercially successful films Disturbia and Surf's Up. The same year he was cast in Michael Bay's science fiction film Transformers as Sam Witwicky, the main protagonist of the series.

Transformers was a box office success and one of the highest-grossing films of 2007. LaBeouf later appeared in its sequels Transformers: Revenge of the Fallen (2009) and Transformers: Dark of the Moon (2011), both also box office successes. In 2008, he played Henry "Mutt Williams" Jones III in Indiana Jones and the Kingdom of the Crystal Skull.

His other credits include the films Holes (2003), Constantine (2005), Wall Street: Money Never Sleeps (2010), Lawless (2012), The Company You Keep (2012), Nymphomaniac (2013), Charlie Countryman (2013), Fury (2014), American Honey (2016), Borg vs McEnroe (2017), Honey Boy (2019), The Peanut Butter Falcon (2019), and Pieces of a Woman (2020).

Since 2014, LaBeouf has pursued a variety of public performance art projects with LaBeouf, Rönkkö & Turner.