Zeitlin was born in Manhattan and raised in Sunnyside, Queens, New York City, and in the suburbs of Hastings-on-Hudson, NY. He is a graduate of Wesleyan University in Middletown, Connecticut. He was born to folklorists Mary Amanda Dargan and Steven Joel "Steve" Zeitlin, who founded City Lore in New York City. His father is Jewish, and his mother, who is from Darlington, South Carolina, comes from a Protestant background.
In 2004, he cofounded the Court 13 independent collection of filmmakers, named after a neglected Wesleyan University squash court that Zeitlin and his friends used as a filming site. He moved to New Orleans while making his first short film, Glory at Sea, in 2008.
In 2012, his first feature, Beasts of the Southern Wild, won the Caméra d'Or award at the Cannes Film Festival, the Grand Jury Prize: Dramatic at the Sundance Film Festival, and the Grand Jury Prize at the Deauville American Film Festival. The film went on to earn the Los Angeles Film Festival's Audience Award for Best Narrative Feature and the Seattle International Film Festival's Golden Space Needle Award for Best Director. Zeitlin was also given a Humanitarian Award for his work on the film at the Satellite Awards 2012.
For his directorial work and screenplay in Beasts, Zeitlin continues to collect additional independent film awards and nominations. At the Gotham Independent Film Awards in 2012, he won the "Breakthrough Director" award. At the same awards ceremony, Zeitlin received the inaugural Bingham Ray Award, which honors the independent filmmaker who died in 2012. Zeitlin also won a Humanitas Prize (as co-writer/director; shared with Lucy Alibar as co-writer), amongst other awards. He has also received nominations for two Academy Awards at the 85th Academy Awards: Best Director and Best Adapted Screenplay (Lucy Alibar, Benh Zeitlin).