Dunne, who had a history of heart trouble, collapsed and died at his New York apartment Tuesday night.
The grandson of an Irish immigrant, Dunne often focused on the Irish-American experience, particularly in his novel "True Confessions." The 1977 breakthrough book involved a Los Angeles murder and its effect on two Irish-Catholic brothers, one a detective, the other a priest, neither untainted by corruption.
Robert De Niro and Robert Duvall starred in the movie, which Dunne adapted with Didion.
"'True Confessions' was a major novel, one of the best books ever written about politics," said Pulitzer Prize winner David Halberstam, a friend and fellow writer. "He was a very important writer, and a wonderful friend - talented, edgy, combative."
Dunne's earlier book "The Studio" offered an unflinching look at the behind-the-scenes machinations at Twentieth Century Fox, a major movie studio. It was hailed for its insider's take on Hollywood.
Dunne eventually became part of the movie industry, working with Didion on several screenplays. Their first, "Panic in Needle Park," starred Al Pacino and captured an award at the 1971 Cannes Film Festival.
Dunne, born in Hartford, Conn., was the fifth of six children. He developed a childhood stutter, and found it easier to express himself in writing.
Dunne graduated from Princeton University in 1954, then joined Time magazine for five years.
He met Didion when she was working at Vogue magazine. They wed in 1964, and soon relocated to her native California to launch careers as freelance writers.
Both wrote for the Saturday Evening Post, with Dunne turning one of his pieces on Cesar Chavez and the grape-pickers strike into a book.
Twentieth Century Fox production head Richard Zanuck gave Dunne approval to spend a year on the studio lot. The result, published in 1969, was acclaimed by critics.
By 1972, after the "Needle Park" effort, Dunne and Didion had developed her novel "Play It as It Lays" into a script.
John Gregory Dunne and Didion also worked on early drafts of "A Star is Born," Barbra Streisand's 1976 rock 'n' roll remake of the classic Judy Garland-James Mason movie. It proved financially lucrative, if not artistically rewarding.
He followed up with critically acclaimed novels like "Dutch Shea, Jr." and "The Red White and Blue."
In 1996, he published a novel about Hollywood, "Playland," and worked with Didion on a screenplay about the life of troubled TV reporter Jessica Savitch. It became "Up Close and Personal," a 1996 movie with Michelle Pfeiffer and Robert Redford that had little in common with the Savitch story.
The Dunne name is well-known in Hollywood. "Needle Park" and "Play It" were both produced by John Gregory Dunne's older brother, Dominick, who is a writer and actor. Dominick's children are famous in their own right: actress Dominique Dunne and actor, director and writer Griffin Dunne.
Dunne was a frequent contributor to The New York Review of Books, and was renowned for his colorful descriptions of writing and the creative process. In a 1986 Esquire article, he called writing "manual labor of the mind: a job, like laying pipe."
Dunne died just after he and his wife returned home from visiting their seriously ill daughter, Quintana Roo, in the hospital.
"My belief is it was all such a strain on his heart," said Dominick Dunne. "He had a pacemaker already. He just sat down, had a heart attack, and died."