Milius studied film at the University of Southern California School of Cinema-Television, where he won first prize in a student film contest for his entry Marcello I'm Bored.
Milius wrote or co-wrote the screenplays for Dirty Harry (uncredited), Jeremiah Johnson (with Edward Anhalt), The Life and Times of Judge Roy Bean, Magnum Force, Apocalypse Now, Geronimo: An American Legend (directed by Walter Hill), and co-writing the story for the Steven Spielberg comedy 1941. He contributed writing to the film adaptations of Tom Clancy's Jack Ryan novels The Hunt for Red October and Clear and Present Danger.
Milius originally planned to limit his career to writing, but his experience with what he considered the mistreatment of his scripts for The Life and Times of Judge Roy Bean and Jeremiah Johnson convinced him he had to become a director if he wanted his vision realized on the screen. He wrote and directed Dillinger, The Wind and the Lion, Big Wednesday, Conan the Barbarian, Red Dawn, Farewell to the King, Flight of the Intruder, the Showtime cable-TV film Motorcycle Gang, and the TNT mini-series Rough Riders.
Milius wrote a number of iconic film quotations such as "Charlie don't surf" and "I love the smell of napalm in the morning," from Apocalypse Now, and the famous Dirty Harry one-liners delivered by Clint Eastwood, including "Go ahead, make my day" and "Do you feel lucky?" Milius also had a hand in the USS Indianapolis monologue in the film Jaws. When Spielberg asked him to punch up the screenplay for Saving Private Ryan, Milius suggested the Normandy cemetery bookends where Ryan, now an elderly hero of World War II, in a moment of survivor guilt, asks his wife "Did I live a good life?"
After his work on Rough Riders (1997), Milius became an instrumental force in lobbying Congress to award President Theodore Roosevelt the Medal of Honor (posthumously), for acts of conspicuous gallantry while in combat on San Juan Hill. Milius made two films featuring Roosevelt: The Wind and the Lion (where he was played by Brian Keith) and the made-for-TV film Rough Riders (where Tom Berenger took the role).
The John Milner character in George Lucas' film American Graffiti was inspired by Lucas' good friend John Milius. (Lucas was Milius' protégé when they were film students together at USC and Milius played a key role in helping Lucas get his start as a director.) Likewise, the Walter Sobchak character in the film The Big Lebowski, made by his friends the Coen Brothers, was based on Milius.
Milius was also instrumental during the startup of the UFC (Ultimate Fighting Championship) organization: it was his idea to use the octagon-shaped cage, and his association with UFC helped provide interest and investors to the startup UFC.
He also created the HBO/BBC television series Rome and a series called Pharaoh.
In 2007, Milius was the recipient of the Austin Film Festival's Distinguished Screenwriter Award.
In March 2011, Milius was a story consultant for the video game Homefront, about a North Korean conquest of America.
Mickey Rourke has been in talks with Milius to bring to star in a biopic of Genghis Khan. Milius has also had talks to adapt the novel Aztec into a miniseries.
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