Brakhage was born as Robert Sanders in an orphanage in Kansas City, Missouri. Two weeks after his birth, he was adopted by Ludwig and Clara Brakhage, and he was given the name James Stanley Brakhage.
As a child, he appeared on radio as a boy soprano before going to high school in Central City, Colorado and then dropping out of Dartmouth College after just two months to make films. He was influeced by the writings of Sergei Eisenstein and the films of Jean Cocteau as well as the Italian neo-realism movement. His first film, Interim (1952), was in the neo-realist style and had music by James Tenney.
In 1954, Brakhage moved to New York City where he associated with a number of contemporary artists, among them the poets Robert Creeley and Kenneth Rexroth and the abstract expressionist painters.
Brakhage's film are usually abstract and lack a traditional story. They are also generally silent, thus emphasising their visual element which Brakhage thought more fundamental to film than sound. His films range in length from just a few seconds to several hours, but most last between two or three minutes and one hour. Most of his work was done in 8mm or 16mm film, and he frequently hand-painted the film or scratched the image directly into the film emulsion, and sometimes used collage techniques. For Mothlight (1963), for example, he stuck moth wings onto tape and made prints from it.
Brakhage's work covers a variety of subjects and techniques. Window Water Baby Moving (1959) is a record of the birth of his first child, while 23rd Psalm Branch (1966-67) intercuts footage of Colorado where he lived with shots of World War II. Dog Star Man (1961-64), perhaps his most famous work, features a man climbing a mountain, shots of stellar objects and more footage of his wife giving birth. It is usually read as addressing the unity of creation.
Brakhage wrote a number of books, including Metaphors on Vision. He often gave lectures at universities, galleries, film festivals and so on. From 1969 he taught film history and aesthetics at the Art Institute of Chicago and from 1981 taught at the University of Colorado.
Brakhage retired to Canada in 2002. He died in Victoria, British Columbia from bladder cancer having made almost four hundred films in all. It is believed that the coal-tar dyes he used to paint his films contributed to the cancer.
Brakhage is revered as one of the most important experimental filmmakers of the 20th century, and his work has had some small impact on mainstream cinema also with the credits of the film Seven, with their scratched emulsion, rapid cutaways and bursts of light, being very much in Brakhage's style.
Among Brakhage's students were the creators of South Park, Matt Stone and Trey Parker. The character Stan in South Park is apparently an homage to Brakhage, in name if nothing else. The opening track of Stereolab's album Dots and Loops, "Brakhage", is also named after him.
After his death, a DVD including 26 of Brakhage's films, by Brakhage, was released by Criterion.