John Churchill was born and raised in Phoenix, Arizona. He attended the University of Colorado at Boulder, receiving degrees in both English Literature and Theatre. He made his professional acting debut on stage at the Colorado Shakespeare Festival, before relocating to Los Angeles.

He has appeared in dozens of films and television series, and has collaborated with such notable, award-winning directors as David Fincher, John Singleton, Chinonye Chukwu, Spike Jonze, Paul Schrader, Todd Field and Tim Van Patten.

John's film credits include his work opposite Gary Oldman in "Mank", his lead role in the independent feature "Evil Takes Root", the Sundance Grand Jury Prize winner "Clemency", and his supporting role in the 2025 Tribeca Film Festival feature "Lemonade Blessing". 

His television credits include, among others, "Beef", "NCIS: Origins", "Monsters: The Lyle and Erik Menendez Story", "Hacks", "S.W.A.T.", "Grey's Anatomy", "DC's Legends of Tomorrow", "Shameless", "Perry Mason" and recurring roles on "CSI" and Nathan Fielder's "The Rehearsal".

He currently resides in Los Angeles with his wife, Danielle, and their two children.