He then gained worldwide fame for his collaborations with Orson Welles on Citizen Kane (1941), The Magnificent Ambersons (1942), and Journey into Fear (1943), in which Cotten starred and for which he was also credited with the screenplay.

[citation needed] 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.

[12] In 1934, Cotten met and became friends with Orson Welles, a fellow cast member on CBS Radio's The American School of the Air.

[4]: 30–31  Welles regarded Cotten as a brilliant comic actor,[13]: 166  and gave him the starring role in his Federal Theatre Project farce, Horse Eats Hat[4]: 34 [14] (September 26 – December 5, 1936).

"[16] 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.

That same year Cotten made his film debut in the Welles-directed short, Too Much Johnson (1938), a comedy that was intended to complement the aborted 1938 Mercury stage production of William Gillette's 1894 play.

[17] 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.

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."

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.

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.

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.

It was a collaborative effort due to the difficulties shooting the film and the pressures related to Welles' imminent departure to South America to begin work on It's All True.

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.

Selznick then put Cotten in the wartime drama Since You Went Away (1944) alongside Claudette Colbert, Jennifer Jones and Shirley Temple, which was another major success.

[24] 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.

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 portrays a writer of pulp fiction who travels to postwar Vienna to meet his friend Harry Lime (Welles).

[27] Years later, Cotten would recall that "Orson Welles lists Citizen Kane as his best film, Alfred Hitchcock opts for Shadow of a Doubt, and Sir Carol Reed chose The Third Man – and I'm in all of them.

"[28] Cotten then reunited with Hitchcock and Ingrid Bergman in Under Capricorn (1949)[21] as an Australian landowner with a shady past; it was a box office disappointment.

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.

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 from November 11, 1953, until August 21, 1954, and was the basis of the Billy Wilder film Sabrina, which starred Humphrey Bogart and Audrey Hepburn.

He made a cameo appearance in Welles's Touch of Evil (1958) and a starring role in the film adaptation of Jules Verne's From the Earth to the Moon (1958).

[39] For the third time, Cotten was in a Broadway hit but did not reprise his role in the film version; Yul Brynner played the part on screen.

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 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) and Cutter's Trail (1970).

[45] He had lead roles in Doomsday Voyage (1972), Baron Blood (1972), and The Scopone Game (1973) and was in The Devil's Daughter (1973),[46] 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), The Perfect Crime (1978), Island of the Fishmen (1979), Concorde Affaire '79 (1979), Guyana: Cult of the Damned (1979), Churchill and the Generals (1979), Tales of the Unexpected and Fantasy Island.

"[49] Cotten's final performances include in George Bower's supernatural horror film The Hearse (1980), the ABC television movie Casino (1980), Michael Cimino's Heaven's Gate (1980), multiple episodes of The Love Boat (1981), The Survivor (1981), shot in Australia and Delusion (1981).

[51][52] He adopted Kipp's daughter, Judith Lenore LaMonte, from her previous marriage who later went on to marry James Pande Young, a television director.

[53] He married British actress Patricia Medina on October 20, 1960, in Beverly Hills at the home of David O. Selznick and Jennifer Jones.