At one stage Milius considered becoming an artist or historian. During a rainy day on a summer vacation in Hawaii in 1962, he stumbled upon a movie theatre showing a week of Akira Kurosawa films and fell in love with cinema.

Milius’s name had been mentioned in a 1968 Time magazine article about the new generation of Hollywood filmmakers, which also referred to George Lucas and Martin Scorsese. This was read by Mike Medavoy, who became Milius’s agent. Medavoy called Milius “a badboy mad genius in a teenager’s body, but he was a good and fast writer with original ideas.”

He followed this with The Last Resort which was optioned by Michael S Laughlin in 1969. Milius says, “Neither of them were ever made, but I was able to option them. I had them rented out for like $5,000 a year.”

Milius sold the script to Warner Bros. in 1970 for $5,000, going up to $50,000 if it was ever made. Eventually, Robert Redford agreed to play the lead and Sydney Pollack signed to direct.

In 1974 David Picker announced he would produce Ranch Life and the Hunting Trail directed by Milius and written by Winfred Blevins, about Theodore Roosevelt. The film was never made. Neither was The Life and Times of Joe McCarthy, a proposed biopic about the famous anti-Communist Senator, which Milius declared interest in making.

In 1975, Milius formed his own production company, The A Team, with Buzz Feitshans, who had edited Dillinger. They had a five-year deal with Warner Bros. Milius said, “Our motto is Civitas Sine Prudentia, which really translates to Social Irresponsibility; I believe in it. It’s refreshing, it’s liberating. Americans are basically socially irresponsible … Who else would have invented the atomic bomb quite the same way? The Nazis would have invented it with the desire to conquer the world; we were the only people that could have invented it with the desire not to conquer the world”

“My religion is surfing”, he said in 1976, adding that “The other thing that influenced me throughout my youth was my involvement with things Japanese. I studied judo, kendo, and painting. I felt more comfortable with things Japanese and with Japanese people than I did with Europeans … feudalism in any country, at any period, fascinates me … I understand the reasoning of people in Asia, it makes sense to me. Zen is very sensible, the whole way of feeling things is logical, whereas many of the Western-motivated things —greed, business sense— I’m not comfortable with, I don’t understand their rationale.”

He did come close to making Extreme Prejudice, based on his script, in 1976. However he decided to make Big Wednesday instead; Extreme Prejudice would be made a decade later, much rewritten, and directed by Walter Hill.

However, the following year saw the release of Apocalypse Now, directed by Francis Ford Coppola. Coppola rewrote the script, which Milius disliked. “He wanted to ruin it, liberalize it, and turn it into Hair”, said Milius in 1976. “He sees himself as a great humanitarian, an enlightened soul who will tell you such wonderful things as he does at the end of Godfather 2 — that crime doesn’t pay … Talent-wise, he’s no John Ford; character-wise, he’s no Steve Spielberg. Francis can’t stand to have any other creative influence around … Francis Coppola has this compelling desire to save humanity when the man is a raving fascist, the Bay Area Mussolini.”

Spielberg said in 1978 that Milius was key to the group of young filmmakers known as the New Hollywood, which included himself, Lucas, and Coppola:

Milius’s old agent, Mike Medavoy, helped establish Orion Pictures in 1978 and one of their first movies was going to be East of Suez, written and directed by Milius. It was not made.

In 1979 Milius said “the ultimate aim of the A Team is that it will become a company that makes lots of projects. I shall be the figurehead and the father figure and take a percentage and I won’t have to do anything except go off and direct my movie once every three years.”

In 1986 it was reported that he was writing the script for Fatal Beauty which he hoped to direct with Cher; the film was made by Tom Holland and starred Whoopi Goldberg.

In 1992 Milius claimed that he was blacklisted for his conservative beliefs in liberal Hollywood, saying that his flops were not as forgiven as those from more leftist directors. “It weighs ten times heavier against me”, he said. “If you don’t share the politically correct vision, then you are an outlaw, you are hunted and there is a price on your head, and if they catch you they will hang you.”

In 1993 he replaced Andrei Konchalovsky as director on The Northmen for Morgan Creek Productions, about an English monk who gets captured by a band of Vikings. “This was inevitable”, Milius said of his directing a Viking film. “I’ve been a practicing pagan for a long time. Conan the Barbarian was really a Viking movie but it was disguised.” However, financing fell through. He was going to direct an adaptation of Tom Clancy’s novel Without Remorse with Gary Sinise and Laurence Fishburne, but the project folded in 1995 two weeks before shooting was to commence due to the financial collapse of Savoy Pictures.

The character of John Milner from the 1973 George Lucas film American Graffiti was inspired by Milius, who was a good friend of Lucas while they were at USC film school. Likewise, the character Walter Sobchak in the 1998 film The Big Lebowski, made by his friends the Coen brothers, was partly based on Milius. The novella Blind Jozef Pronek and Dead Souls by Aleksandar Hemon features an episode with Milius, who is described as “sitting at a desk sucking on a cigar as long as a walking stick”.

In 2000 Milius was hired to work as a creative consultant with the Institute for Creative Technologies to pre-visualize the challenges to peace that America will face and the advanced virtual reality technologies necessary to train U.S. troops for the future. “Through his enormous body of work, John has shown a deep understanding of the human condition and the ways that conflict can be resolved”, said ICT executive director Richard Lindheim. “Furthermore our efforts will benefit greatly from his vision of the world in the near future, and the techniques and procedures that will be needed to maintain security.”

Milius has long claimed to be an outsider in Hollywood. In 2001 he stated:

In 2007, Milius was the recipient of the Austin Film Festival’s Distinguished Screenwriter Award. In his acceptance speech, he said that his favorites of his films were The Wind and the Lion, Big Wednesday, and Conan.

In 2010 Milius was working on a new project, a film biography of Genghis Khan, and a proposed TV series called Pharaoh, set during the reign of Queen Hatshepsut, when he had a stroke. For a while he was unable to speak or move, but ultimately he recovered.

In March 2011, Milius was a story consultant for the video game Homefront, about a North Korean conquest of America.

In 2013, a documentary about his life, titled Milius, was released.