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John Hamburg was born and raised in New York City, and began making short films while still in high school. He continued creating films while attending Brown University, where he also studied playwriting and, later, at New York University's Tisch School of the Arts. While at Tisch, he wrote and directed the short film Tick, which debuted at the 1996 Sundance Film Festival.

In 1998, he returned to Sundance with his feature-length debut Safe Men, a comedy he wrote and directed. Starring Sam Rockwell, Steve Zahn, Paul Giamatti, Mark Ruffalo and Harvey Fierstein, Hamburg's film about safecrackers and song-writers in Providence, Rhode Island has garnered a strong cult following in the years since its Sundance premiere.

He next co-wrote the screenplays for the popular comedies Meet the Parents starring frequent collaborator Ben Stiller, Robert De Niro, Blythe Danner and Terri Polo and Zoolander starring Stiller and Owen Wilson. Hamburg also directed several episodes of the critically acclaimed television series Undeclared.

Hamburg next wrote and directed the hit comedy Along Came Polly starring Ben Stiller, Jennifer Aniston, Alec Baldwin and Philip Seymour Hoffman, and co-wrote the successful sequel Meet the Fockers starring Ben Stiller, Robert De Niro, Dustin Hoffman and Barbra Streisand, both for Universal Pictures.