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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.

(Welles and Cotten remained close friends until Welles's death in 1985. According to Welles, Cotten was always uncomfortable as a leading man and preferred to play supporting or character roles.)

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.

Cotten was portrayed by Tim Robbins in the 1985 TV film Malice in Wonderland, James Tupper in the film Me and Orson Welles (2008) and by Matthew Glave in the television series Feud (2017), which depicts the filming of Hush...Hush, Sweet Charlotte.

On June 8, 1981, Cotten experienced a heart attack followed by a stroke that affected his brain's 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. When Cotten announced he had written a book, Welles asked for the manuscript and read it that night.

Cotten's final performances included The Hearse (1980), Casino (1980), Heaven's Gate (1980), The Love Boat (1981), The Survivor (1981), shot in Australia, and Delusion (1981). Cotten suffered a stroke in 1981 which caused him to temporarily lose his voice.

He had lead roles in Doomsday Voyage (1972), Baron Blood (1972), and The Scopone Game (1973) and was in The Devil's Daughter (1973), The Streets of San Francisco, Soylent Green (1973), A Delicate Balance (1973), The Rockford Files, Syndicate Sadists (1975), The Timber Tramps (1975), The Lindbergh Kidnapping Case (1976), A Whisper in the Dark (1976), Origins of the Mafia (1976), Twilight's Last Gleaming (1977) for Aldrich, Airport '77, Aspen (1977), The Hardy Boys/Nancy Drew Mysteries, Last In, First Out (1978), Caravans (1978), Indagine su un delitto perfetto (1978), Screamers (1979), Concorde Affaire '79 (1979), Guyana: Cult of the Damned (1979), Churchill and the Generals (1979), Tales of the Unexpected and Fantasy Island.

Cotten was in The Name of the Game, It Takes a Thief, NET Playhouse, The Grasshopper (1970), Tora! Tora! Tora!, The Virginian, Assault on the Wayne (1971), Do You Take This Stranger? (1971), City Beneath the Sea (1971), The Abominable Dr. Phibes (1971), Lady Frankenstein (1971), and The Screaming Woman (1972) with de Havilland.

He guest starred on Cimarron Strip, Ironside, and Journey to the Unknown and had a support role in Jack of Diamonds (1967). He had the lead in White Comanche (1968) and Latitude Zero (1969) (shot in Japan with his wife) and supported in the TV movies The Lonely Profession (1969), Cutter's Trail (1970).

Cotten was top billed in The Great Sioux Massacre (1965) and The Tramplers (1965), but back to support parts for The Money Trap (1965) and The Oscar (1966). He was top billed in Brighty of the Grand Canyon (1966), directed by Foster, The Cruel Ones (1967), Some May Live (1967) and Gangsters '70 (1968).

Cotten returned to Broadway to appear in Calculated Risk (1962–63), which ran for 221 performances and meant he had to turn down a role in a film Harrigan's Halo. He guest starred on The Great Adventure, and 77 Sunset Strip, and did the pilot Alexander the Great (1963).

In 1960, Cotten married British actress Patricia Medina after his first wife, Lenore Kipp, died of leukemia earlier in the year.

Cotten had a supporting role in the films The Angel Wore Red (1960) and The Last Sunset (1961), the latter directed by Robert Aldrich, and guest starred on The DuPont Show with June Allyson, Checkmate, The Barbara Stanwyck Show, Bus Stop, Theatre '62 (an adaptation of Notorious), Dr. Kildare, Wagon Train, and Saints and Sinners.

He guest starred on Jane Wyman Presents The Fireside Theatre, Telephone Time, Playhouse 90, Schlitz Playhouse, Zane Grey Theater, Suspicion, and Westinghouse Desilu Playhouse. 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).

Cotten had another success on Broadway when he appeared in Once More, With Feeling (1958–60) which ran for 263 performances. For the third time Cotten was in a Broadway hit but did not reprise his role in the film version – Yul Brynner did.

In 1956, Cotten starred in the NBC anthology series On Trial (renamed at mid-season The Joseph Cotten Show). It ran for 41 episodes.

He returned to features with The Bottom of the Bottle (1956), The Killer Is Loose (1957) and The Halliday Brand (1957).

Cotten made Special Delivery (1955) in West Germany, did a TV adaptation of Broadway for The Best of Broadway (1955) directed by Franklin J. Schaffner. He appeared in episodes of Celebrity Playhouse, The Ford Television Theatre, Star Stage, Alfred Hitchcock Presents (several times) and General Electric Theater.

In 1955 Cotten hosted The 20th Century Fox Hour on television.

Cotten did a Western at Universal, Untamed Frontier (1953), during the filming of which he was injured. He did a thriller for Andrew L. Stone, The Steel Trap (1952), which reunited with Teresa Wright from Shadow of a Doubt.

At Fox he was in the Marilyn Monroe vehicle Niagara (1953), after James Mason turned down the role. He narrated Egypt by Three (1953) and was reunited with Stone in A Blueprint for Murder (1953).

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. He and Sullivan did a TV production of State of the Union for Producers' Showcase directed by Arthur Penn.

At Fox he did Half Angel (1951) with Young, then did another with Wallis at Paramount, Peking Express (1951) and went to MGM for The Man with a Cloak (1951) with Barbara Stanwyck. He had a cameo in Welles' Othello (1951).

Cotten co-starred with Joan Fontaine in September Affair (1950) for Hal Wallis. Selznick loaned him to 20th Century Fox for the dark Civil War Western Two Flags West (1950), then to RKO for Walk Softly, Stranger (1950, shot in 1948) which reunited him with Alida Valli from The Third Man. It was a huge flop.

Cotten was reunited with Welles in The Third Man (1949), produced by Korda and Selznick. Cotten portrays a writer of pulp fiction who travels to postwar Vienna to meet his friend Harry Lime (Welles). When he arrives, he is told that Lime has died. Determined to prove to the police that his friend was murdered, he uncovers an even darker secret.

Cotten then reunited with Hitchcock and Ingrid Bergman in Under Capricorn (1949) as an Australian landowner with a shady past; it was a box office disappointment. So too was Beyond the Forest (1949) with Bette Davis at Warner Bros.

At the 10th Venice International Film Festival, Cotten was given the Volpi Cup for Best Actor for his performance in the film Portrait of Jennie (1948). He was also given a star on the Hollywood Walk of Fame in 1960.

Dore Schary, who had worked for Selznick, went to run RKO and hired Cotten for The Farmer's Daughter (1947), where he was Loretta Young's leading man. Cotten then made Portrait of Jennie (1948) for Selznick, co starring with Jones; Cotten played a melancholy artist who becomes obsessed with a girl who might have died many years before. His performance won Cotten the International Prize for Best Actor at the 1949 Venice International Film Festival.

Selznick used Cotten, Jennifer Jones and Gregory Peck in Duel in the Sun (1946), an epic Western that was hugely popular at the box office.

Selznick followed this up by teaming Cotten with Ginger Rogers and Temple in I'll Be Seeing You (1945), another melodrama. Hal Wallis borrowed Cotten and Jones to make Love Letters (1945). Exhibitors voted him the 17th most popular star in the United States in 1945.

Selznick loaned out Cotten and Ingrid Bergman to MGM for the thriller Gaslight (1944) which was a major hit. Selznick then put Cotten in a wartime drama Since You Went Away (1944) alongside Claudette Colbert, Jennifer Jones and Shirley Temple; it was another major success.

Cotten was cast in the Nazi-related thriller Journey into Fear (1943) based on the novel by Eric Ambler. It was originally scripted by Ben Hecht but Welles, who was supervising, disliked it, and he rewrote it with Cotten. 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.

Alfred Hitchcock hired Cotten to play a charming serial killer in Shadow of a Doubt (1943). It was made for Universal Pictures, who for whom Cotten then appeared in Hers to Hold (1943), as Deanna Durbin's leading man.

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!" Cotten signed a long term deal with Selznick.

Cotten starred in Welles's adaptation and production of The Magnificent Ambersons (1942). 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.

He first gained worldwide fame in three Orson Welles films: Citizen Kane (1941), The Magnificent Ambersons (1942), and Journey into Fear (1943), for which Cotten was also credited with the screenplay. He went on to become one of the leading Hollywood actors of the 1940s, appearing in films such as Shadow of a Doubt (1943), Love Letters (1945), Duel in the Sun (1946), Portrait of Jennie (1948), The Third Man (1949) and Niagara (1953). One of his final films was Michael Cimino's Heaven's Gate (1980).

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.

Alexander Korda then hired Cotten to play Merle Oberon's leading man in Lydia (1941). "I didn't care about the movies, really," Cotten said later. "I was tall. I had curly hair. I could talk. It was easy to do."

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.

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 417 performances 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."

He followed it with The Shoemaker's Holiday (1938) and Danton's Death (1938) for Welles. Cotten also performed 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.

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 1937, Cotten became an inaugural member of Welles's Mercury Theatre company, starring in its Broadway productions Caesar as Publius; it ran for 157 performances.

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.

He followed it with Jezebel (1933), staged by Katherine Cornell and Guthrie McClintic, which only had a short run.

Cotten struggled to find work in the depression so turned to modeling and acting in industrial films. He also performed on radio. Cotten made his Broadway debut in 1932 in Absent Friends which ran for 88 performances.

He moved to Miami in 1925 and worked as an advertising salesman for The Miami Herald at $35 a week. He started performing at the Miami Civic Theatre, and worked there for five years, also reviewing the shows for the Herald.

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.

Joseph Cheshire Cotten Jr. (May 15, 1905 – February 6, 1994) was an American film, stage, radio and television actor. Cotten achieved prominence on Broadway, starring in the original stage productions of The Philadelphia Story and Sabrina Fair.

Joseph Cotten was born in 1905 in Petersburg, Virginia, the first of three boys born for 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.