Joseph Cotten was born in 1905 in Petersburg, Virginia, the first of three sons born to Joseph Cheshire Cotten, Sr., an assistant postmaster, and Sally Willson Cotten. He grew up in the Tidewater region and showed an aptitude for drama and a gift for storytelling. In 1923, when Cotten was 18, his family arranged for him to receive private lessons at the Hickman School of Expression in Washington, D.C., and underwrote his expenses. He earned spending money playing professional football on Sundays, for $25 a quarter. After graduation, he earned enough money as a lifeguard at Wilcox Lake to pay back his family's loan, with interest.
He worked as an advertising agent, and his work as a theatre critic inspired him to become involved in theatre productions, first in Virginia, then in New York City. Cotten made his Broadway debut in 1930.
In 1934, Cotten met and became friends with Orson Welles, a fellow cast member on CBS Radio's The American School of the Air. Welles regarded Cotten as a brilliant comic actor, and gave him the starring role in his Federal Theatre Project farce, Horse Eats Hat (September 26 – December 5, 1936). Cotten was sure that Horse Eats Hat won him the notice of his future Broadway co-star, Katharine Hepburn.
In 1937, Cotten became an inaugural member of Welles's Mercury Theatre company, starring in its Broadway productions Caesar, The Shoemaker's Holiday and Danton's Death, and in radio dramas presented on The Mercury Theatre on the Air and The Campbell Playhouse.
Cotten made his film debut in the Welles-directed short, Too Much Johnson, a comedy that was intended to complement the aborted 1938 Mercury stage production of William Gillette's 1890 play. The film was never screened in public and was lost until 2013.
Cotten returned to Broadway in 1939, creating the role of C. K. Dexter Haven opposite Katharine Hepburn's Tracy Lord in the original production of Philip Barry's The Philadelphia Story. The play ran for a year at the Shubert Theatre, and in the months before its extensive national tour a film version was to be made by MGM. Cotten went to Hollywood, but discovered there that his stage success in The Philadelphia Story translated to, in the words of his agent Leland Hayward, "spending a solid year creating the Cary Grant role." Hayward suggested that they call Cotten's good pal, Orson Welles. "He's been making big waves out here," Hayward said. "Maybe nobody in Hollywood ever heard of the Shubert Theatre in New York, but everybody certainly knows about the Mercury Theatre in New York."
After the success of Welles's War of the Worlds 1938 Halloween radio broadcast, Welles gained a unique contract with RKO Pictures. The two-picture deal promised full creative control for the young director below an agreed budget limit, and Welles's intention was to feature the Mercury Players in his productions. Shooting had still not begun on a Welles film after a year, but after a meeting with writer Herman J. Mankiewicz Welles had a suitable project.
In mid-1940, filming began on Citizen Kane, portraying the life of a press magnate (played by Welles) who starts out as an idealist but eventually turns into a corrupt, lonely old man. The film featured Cotten prominently in the role of Kane's best friend Jedediah Leland, eventually a drama critic for one of Kane's papers.
When released on May 1, 1941, Citizen Kane — based in part on the life of William Randolph Hearst — did not do much business at theaters; Hearst owned numerous major newspapers, and forbade them to carry advertisements for the film. Nominated for nine Academy Awards in 1942, the film won only for Best Screenplay, for Mankiewicz and Welles. Citizen Kane launched the film careers of the Mercury Players, including Agnes Moorehead (who played Kane's mother), Ruth Warrick (Kane's first wife), and Ray Collins (Kane's political opponent). However, Cotten was the only one of the four to find major success as a lead in Hollywood outside of Citizen Kane; Moorehead and Collins became successful character film actors and Warrick spent decades in a career in daytime television.
Cotten starred a year later in Welles's adaptation and production of The Magnificent Ambersons. After the commercial disappointment of Citizen Kane, RKO was apprehensive about the new film, and after poor preview responses, cut it by nearly an hour before its release. Though at points the film appeared disjointed, it was well received by critics. Despite the critical accolades Cotten received for his performance, he was again snubbed by the Academy.
Cotten and Welles (uncredited) wrote the Nazi-related thriller Journey into Fear (1943) based on the novel by Eric Ambler. Released by RKO, the Mercury production was directed by Norman Foster. It was a collaborative effort due to the difficulties shooting the film and the pressures related to Welles's imminent departure to South America to begin work on It's All True.
After Welles's return he and Cotten co-produced The Mercury Wonder Show for members of the U.S. armed services. Opening August 3, 1943, the all-star magic and variety show was presented in a tent at 9000 Cahuenga Boulevard in Hollywood. Featured were Welles (Orson the Magnificent), Cotten (Jo-Jo the Great), Rita Hayworth (forced to quit by Columbia Pictures boss Harry Cohn and replaced by Marlene Dietrich), Agnes Moorehead (Calliope Aggie) and others. Tickets were free to servicemen, and more than 48,000 of them had seen show by September 1943.
In late 1943, Cotten visited Welles's office and said that producer David O. Selznick wanted to make two or three films with him, but that he wanted him under his own contract. Welles then tore up Cotten's contract with Mercury Productions, saying, "He can do more for you than I can. Good luck!"
In film, Cotten and Welles worked together in The Third Man (1949). Cotten portrays a writer of pulp fiction who travels to postwar Vienna to meet his friend Harry Lime (Welles). When he arrives, he discovers that Lime has died, and is determined to prove to the police that it was murder, but uncovers an even darker secret.
The characters that Cotten played onscreen during the 1940s ranged from a serial killer in Hitchcock's Shadow of a Doubt (1943) to an eager police detective in Gaslight (1944). Cotten starred with Jennifer Jones in four films for Selznick International Pictures: the wartime domestic drama Since You Went Away (1944); the romantic drama Love Letters (1945); Duel in the Sun (1946), which remains one of the top 100 highest-grossing films of all time when adjusted for inflation; "The Farmer's Daughter" and the critically acclaimed Portrait of Jennie (1948), in which he played a melancholy artist who becomes obsessed with a girl who may have died many years before. As well as reuniting onscreen with Orson Welles in Carol Reed's The Third Man in 1949, he reunited with Hitchcock in Under Capricorn (1949) as an Australian landowner with a shady past.
Exhibitors voted him the 17th most popular star in the United States in 1945.
Cotten's screen career cooled in the 1950s with a string of less high-profile roles in films such as the dark Civil War Western Two Flags West (1950), the Joan Fontaine romance September Affair (1950), and the Marilyn Monroe vehicle Niagara (1953), after James Mason turned down the role. His last theatrical releases in the 1950s were mostly film-noir and unsuccessful character studies.
On the stage in 1953, Cotten created the role of Linus Larrabee, Jr., in the original Broadway production of Sabrina Fair, opposite Margaret Sullavan. The production ran November 11, 1953 – August 21, 1954, and was the basis of the Billy Wilder film Sabrina, which starred Humphrey Bogart and Audrey Hepburn.
In 1956, Cotten left film for years for a string of successful television ventures, such as the NBC series On Trial (renamed at mid-season The Joseph Cotten Show).
Cotten was featured in Alfred Hitchcock Presents and Ronald Reagan's General Electric Theater. He appeared on May 2, 1957, on NBC's comedy variety series, The Ford Show, Starring Tennessee Ernie Ford. Near the end of the decade, he made a cameo appearance in Welles'sTouch of Evil (1958) and a starring role in the film adaptation of Jules Verne's From the Earth to the Moon (also 1958). He also appeared as Dick Burlingame and Charles Lawrence in the 1960 episodes "The Blue Goose" and "Dark Fear" of CBS's anthology series The DuPont Show with June Allyson. He also appeared on NBC's anthology series, The Barbara Stanwyck Show.
In 1960, Cotten married British actress Patricia Medina after his first wife, Lenore Kipp, died of leukemia earlier in the year. After some time away from film, Cotten returned in the horror classic Hush… Hush, Sweet Charlotte (1964), with Bette Davis, Olivia de Havilland and Agnes Moorehead. The rest of the decade found Cotten in a number of European and Japanese productions, B-movies and made for television movies. He made multiple guest appearances on The Ed Sullivan Show. In 1967, he joined Karl Swenson, Pat Conway, and Dick Foran in the nostalgic western dramatic film Brighty of the Grand Canyon, about a burro who lived in the Grand Canyon of the Colorado River from about 1892–1922. On television, he narrated David L. Wolper's documentary Hollywood and the Stars (1963–64). In 1968 he made a guest appearance in a two-part episode of the series Ironside ("Split Second to an Epitaph").
In the early 1970s, Cotten followed a supporting role in Tora! Tora! Tora! (1970) with several horror features: The Abominable Dr. Phibes (1971) with Vincent Price, and Soylent Green (1973), the last film featuring Edward G. Robinson. Later in the decade, Cotten was in several all-star disaster films, including Airport '77 (1977) with James Stewart and again with Olivia de Havilland, and the nuclear thriller Twilight's Last Gleaming (1977). On television, he did guest spots on The Rockford Files ("This Case Is Closed", 1974) and "The Love Boat".
One of Cotten's last films was the box-office bomb Heaven's Gate (1980), at the time critically mauled in the United States but well received abroad. The film was positively reevaluated early in the 21st century, receiving a Criterion Collection release in 2013.
He appeared in two episodes of a twist-in-the-tale episode of the British television series Tales of the Unexpected, with Wendy Hiller (1979), and Gloria Grahame (1980). He also appeared in three horror films, The Hearse (1980), Delusion (also known as The House Where Death Lives) (1980), and the Australian film The Survivor (1981). Cotten suffered a stroke in 1981 which caused him to temporarily lose his voice.
On June 8, 1981, Cotten had a heart attack followed by a stroke that affected his speech center. He began years of therapy which in time made it possible for him to speak again. As he began to recover, he and Orson Welles talked on the phone each week for a couple of hours: "He was strong and supportive," Cotten wrote, "and whenever I used the wrong word (which was frequently) he would say, 'That's a much better word, Jo, I'm going to use it.'" He and Welles would meet for lunch and reminisce, and when Cotten said he had written a book Welles asked for the manuscript and read it that same night. In a phone conversation on October 9, 1985, Welles told his friend and mentor Roger Hill that Cotten had written a book, and Hill asked how it read. "Gentle, witty, and self-effacing, just like Jo," Welles replied. "My only complaint is that it's too brief." Welles died the following day. "Somewhere among his possessions is a manuscript of this book," Cotten wrote on the last page of his autobiography, published in 1987 under the title Vanity Will Get You Somewhere.
In 1990, Cotten's larynx was removed due to cancer. He died on February 6, 1994, of pneumonia, at the age of 88. He was buried at Blandford Cemetery in Petersburg, Virginia.
Joseph Cotten received a Venice Film Festival Award for Best Actor for his work in Portrait of Jennie.