Avedon attended DeWitt Clinton High School in Bedford Park, Bronx, where from 1937 until 1940 he worked on the school paper, The Magpie, with James Baldwin. As a teen he also won a Scholastic Art and Writing Award. After graduating from DeWitt Clinton that year he enrolled at Columbia University to study philosophy and poetry but dropped out after one year. He then started as a Photographer for the Merchant Marines, taking ID shots of the crewmen with the Rolleiflex camera his father had given him as a gift. From 1944 to 1950 Avedon studied photography with Alexey Brodovitch at his Design Laboratory at The New School for Social Research.
In 1944, Avedon married 19-year-old bank Teller Dorcas Marie Nowell who later became the model and Actress Doe Avedon; they did not have children and divorced in 1949. The couple summered at the gay village of Cherry Grove, Fire Island, and Avedon's bisexuality has been attested to by colleagues and family. Still, he was devastated when Nowell left him.
In 1946, Avedon had set up his own studio and began providing images for magazines including Vogue and Life. He soon became the chief Photographer for Harper's Bazaar. From 1950 he also contributed photographs to Life, Look and Graphis and in 1952 became Staff Editor and Photographer for Theatre Arts Magazine. Avedon did not conform to the standard technique of taking studio fashion photographs, where Models stood emotionless and seemingly indifferent to the camera. Instead, Avedon showed Models full of emotion, smiling, laughing, and, many times, in action in outdoor settings which was revolutionary at the time. However, towards the end of the 1950s he became dissatisfied with daylight photography and open air locations and so turned to studio photography, using strobe lighting.
Hepburn was Avedon's muse in the 1950s and 1960s, and he went so far as to say: "I am, and forever will be, devastated by the gift of Audrey Hepburn before my camera. I cannot lift her to greater heights. She is already there. I can only record. I cannot interpret her. There is no going further than who she is. She has achieved in herself her ultimate portrait."
Hollywood presented a fictional account of Avedon's early career in the 1957 musical Funny Face, starring Fred Astaire as the fashion Photographer "Dick Avery." Avedon supplied some of the still photographs used in the production, including its most noted single image: an intentionally overexposed close-up of Audrey Hepburn's face in which only her noted features – her eyes, her eyebrows, and her mouth – are visible.
In addition to his continuing fashion work, by the 1960s Avedon was making studio portraits of civil rights workers, politicians and cultural dissidents of various stripes in an America fissured by discord and violence. He branched out into photographing patients of mental hospitals, the Civil Rights Movement in 1963, protesters of the Vietnam War, and later the fall of the Berlin Wall.
A personal book called “Nothing Personal,” with a text by his high school classmate James Baldwin appeared in 1964. During this period, Avedon also created two well known sets of portraits of The Beatles. The first, taken in mid to late 1967, became one of the first major rock poster series, and consisted of five psychedelic portraits of the group — four heavily solarized individual color portraits and a black-and-white group portrait taken with a Rolleiflex camera and a normal Planar lens. The next year he photographed the much more restrained portraits that were included with The Beatles LP in 1968. Among the many other rock bands photographed by Avedon, in 1973 he shot Electric Light Orchestra with all the members exposing their bellybuttons for recording, On the Third Day.
Avedon's mural groupings featured emblematic figures: Andy Warhol with the players and stars of The Factory; The Chicago Seven, political radicals charged with conspiracy to incite riot at the 1968 Democratic National Convention; the Beat poet Allen Ginsberg and his extended family; and the Mission Council, a group of military and government officials who governed the United States' participation in the Vietnam War.
In 1970, Avedon purchased a former carriage house on the Upper East Side of Manhattan that would serve as both his studio and apartment. In the late 1970s, he purchased a four-bedroom house on a 7.5-acre (3.0 ha) estate in Montauk, New York, between the Atlantic Ocean and a nature preserve; he sold it for almost $9 million in 2000.
When Diana Vreeland left Harper's Bazaar for Vogue in 1962, Avedon joined her as a staff Photographer. He proceeded to become the lead Photographer at Vogue and photographed most of the covers from 1973 until Anna Wintour became Editor in chief in late 1988. Notable among his fashion advertisement series are the recurring assignments for Gianni Versace, beginning with the spring/summer campaign 1980. He also photographed the Calvin Klein Jeans campaign featuring a fifteen-year-old Brooke Shields, as well as directing her in the accompanying television commercials. Avedon first worked with Shields in 1974 for a Colgate toothpaste ad. He shot her for Versace, 12 American Vogue covers and Revlon's Most Unforgettable Women campaign. In the February 9, 1981, issue of Newsweek, Avedon said that "Brooke is a lightning rod. She focuses the inarticulate rage people feel about the decline in contemporary morality and destruction of innocence in the world." On working with Avedon, Shields told Interview magazine in May 1992 "When Dick walks into the room, a lot of people are intimidated. But when he works, he's so acutely creative, so sensitive. And he doesn't like it if anyone else is around or speaking. There is a mutual vulnerability, and a moment of fusion when he clicks the shutter. You either get it or you don't".
In 1982 Avedon produced a playfully inventive series of advertisements for fashion label Christian Dior, based on the idea of film stills. Featuring Director Andre Gregory, Photographer Vincent Vallarino and model/actress Kelly Le Brock, the color photographs purported to show the wild antics of a fictional "Dior family" living ménage à trois while wearing elegant fashions.
Avedon became the first staff Photographer for The New Yorker in 1992, where his post-apocalyptic, wild fashion fable “In Memory of the Late Mr. and Mrs. Comfort,” featuring model Nadja Auermann and a skeleton, was published in 1995. Other pictures for the magazine, ranging from the first publication, in 1994, of previously unpublished photos of Marilyn Monroe to a resonant rendering of Christopher Reeve in his wheelchair and nude photographs of Charlize Theron in 2004, were topics of wide discussion. Some of his less controversial New Yorker portraits include those of Saul Bellow, Hillary Clinton, Toni Morrison, Derek Walcott, John Kerry, and Stephen Sondheim. In his later years, he continued to contribute to Egoïste, where his photographs appeared from 1984 through 2000. In 1999, Avedon shot the cover photos for Japanese-American singer Hikaru Utada's Addicted to You.
The Richard Avedon Foundation is a private operating foundation, structured by Avedon during his lifetime. It began its work shortly after his death in 2004. Based in New York, the foundation is the repository for Avedon's photographs, negatives, publications, papers, and archival materials. In 2006, Avedon's personal collection was shown at the Pace/MacGill Gallery, New York, and at the Fraenkel Gallery, San Francisco, and later sold to benefit the Avedon Foundation. The collection included photographs by Martin Munkacsi, Edward Steichen and Man Ray, among others. A slender volume, Eye of the Beholder: Photographs From the Collection of Richard Avedon (Fraenkel Gallery), assembles the majority of the collection in a boxed set of five booklets: “Diane Arbus,” “Peter Hujar”, “Irving Penn”, “The Countess de Castiglione” and “Etcetera,” which includes 19th- and 20th-century Photographers.
In 2010, a record price of £719,000 was achieved at Christie's for a unique seven-foot-high print of model Dovima, posing in a Christian Dior evening dress with elephants from the Cirque d’Hiver, Paris, in 1955. This particular print, the largest of this image, was made in 1978 for Avedon’s fashion retrospective at the Metropolitan Museum of Art in New York, and was bought by Maison Christian Dior.
Photographer Annie Leibovitz names Avedon as a major influence, describing his style as ‘personal reportage’, developing close rapport with one's subjects.