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Eisenberg debuted on television with the short-lived comedy-drama  Get Real (1999–2000). Following his first leading role in the film Roger Dodger (2002), he starred in films such as The Squid and the Whale (2005), Adventureland(2009) and Zombieland (2009). He gained wider recognition for starring as Facebook founder Mark Zuckerberg in David Fincher's film The Social Network (2010), for which he was nominated for the Academy Award for Best Actor. Eisenberg then starred in the Woody Allen films To Rome with Love (2012) and Café Society (2016), the heist films Now You See Me (2013) and its 2016 sequel, and independent dramas such as The Double (2013).

He portrayed Lex Luthor in the superhero film Batman v Superman: Dawn of Justice (2016) and had a lead voice role in the animated films Rio(2011) and Rio 2 (2014). In 2022, he starred in the FX / Hulu miniseries Fleishman Is in Trouble. He made his film directorial debut with the black comedy When You Finish Saving the World. He has since directed, written, and starred in A Real Pain (2024), which earned him a nomination for the Academy Award for Best Original Screenplay.

Eisenberg has contributed pieces to  The New Yorker and McSweeney's websites. He has written and starred in three plays for the New York stage: Asuncion, The Revisionist, and The Spoils. He released his first book, Bream Gives Me Hiccups: and Other Stories in 2015.