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Later sound films (1935–1970)

In 1934, Hawks went to Columbia Pictures to make his first screwball comedy, Twentieth Century, starring John Barrymore and Hawks's distant cousin Carole Lombard. It was based on a stage play by Hecht and Charles MacArthur and, along with Frank Capra 's It Happened One Night (released the same year), is considered to be the defining film of the screwball comedy genre. In 1935, Hawks made Barbary Coast with Edward G. Robinson and Miriam Hopkins. Hawks collaborated with Hecht and MacArthur on Barbary Coast and reportedly convinced them to work on the film by promising to teach them a marble game. They would switch off between working on the script and playing with marbles during work days. In 1936, he made the aviation adventure Ceiling Zero with James Cagney and Pat O'Brien. Also in 1936, Hawks began filming Come and Get It, starring Edward Arnold, Joel McCrea, Frances Farmer and Walter Brennan. But he was fired by Samuel Goldwyn in the middle of shooting, and the film was completed by William Wyler.

In 1938, Hawks made screwball comedy Bringing Up Baby for RKO Pictures. It starred Cary Grant and Katharine Hepburn and was adapted by Dudley Nichols and Hagar Wilde. It has been called "the screwiest of the screwball comedies" by Andrew Sarris. Grant plays a near-sighted paleontologist who suffers one humiliation after another due to the lovestruck socialite played by Hepburn. Hawks's artistic direction for Bringing Up Baby revolved around the raw natural chemistry between Grant and Hepburn. With Grant portraying the paleontologist and Hepburn as an heiress, the roles only add to the movie's purpose of disintegrating the line between the real and the imaginary. Bringing Up Baby was a box office flop when initially released and, subsequently, RKO fired Hawks due to extreme losses; however, the film has become regarded as one of Hawks's masterpieces. Hawks followed this with 11 consecutive hits up to 1951, starting with the aviation drama Only Angels Have Wings, made in 1939 for Columbia Pictures and starring Grant, Jean Arthur, Thomas Mitchell, Rita Hayworth and Richard Barthelmess.

In 1940, Hawks returned to the screwball comedy with His Girl Friday, starring Grant and Rosalind Russell. The film was an adaptation of the hit Broadway play The Front Page by Hecht and MacArthur, which had already been made into a film in 1931. Not forgetting the influence Jesse Lasky had on his early career, in 1941, Hawks made Sergeant York, starring Gary Cooper as a pacifist farmer who becomes a decorated World War I soldier. Hawks directed the film and cast Cooper as a specific favor to Lasky. This was the highest-grossing film of 1941 and won two Academy Awards (Best Actor and Best Editing), as well as earning Hawks his only nomination for Best Director. Later that year, Hawks worked with Cooper again for Ball of Fire, which also starred Barbara Stanwyck. The film was written by Billy Wilder and Charles Brackett and is a playful take on Snow White and the Seven Dwarfs. Cooper plays a sheltered, intellectual linguist who is writing an encyclopedia with six other scientists, and hires street-wise Stanwyck to help them with modern slang terms. In 1941, Hawks began work on the Howard Hughes-produced (and later directed) film The Outlaw, based on the life of Billy the Kid and starring Jane Russell. Hawks completed initial shooting of the film in early 1941, but due to perfectionism and battles with the Hollywood Production Code, Hughes continued to re-shoot and re-edit the film until 1943, when it was finally released with Hawks uncredited as director.

After making the World War II film Air Force (1943), starring John Garfield and written by Nichols, Hawks did two films with Humphrey Bogart and Lauren Bacall. To Have and Have Not, made in 1944, stars Bogart, Bacall and Brennan and is based on a novel by Ernest Hemingway. Hawks was a close friend of Hemingway and made a bet with the author that he could make a good film out of Hemingway's "worst book". Hawks, William Faulkner and Jules Furthman collaborated on the script, about an American fishing boat captain working out of Martinique after the Fall of France in 1940. Bogart and Bacall fell in love on the set of the film and married soon afterwards. The greatest strength of the movie has been said to come from its atmosphere and use of wit that really plays on the strengths of Bacall and helps the movie solidify the theme of beauty in perpetual opposition. To Have and Have Not is the only film with contributions from two Nobel laureates, Hemingway and Faulkner. Hawks reunited with Bogart and Bacall in 1945 and 1946 with The Big Sleep, based on the Philip Marlowe detective novel by Raymond Chandler. An early 1945 version was substantially recut to comprise the final 1946 U.S. release with additional scenes emphasizing the special repartee chemistry between Bogart and Bacall. The screenplay for the film also reteamed Faulkner and Furthman, in addition to Leigh Brackett. Chandler, who had been nominated for an Oscar as co-author of the 1944 Double Indemnity screenplay, was not invited to help adapt his best selling novel. The plot is notoriously convoluted; Hawks recalled that "I never figured out what was going on, but I thought the basic thing had great scenes in it, and was good entertainment. After that I said, 'I'm never going to worry about being logical again.'"

In 1948, Hawks made Red River, an epic Western reminiscent of Mutiny on the Bounty starring John Wayne and Montgomery Clift in his first film. Later that year, Hawks remade his Ball of Fire as A Song Is Born, this time starring Danny Kaye and Virginia Mayo. This version follows the same plot but pays more attention to popular jazz music and includes such jazz legends as Tommy Dorsey, Benny Goodman, Louis Armstrong, Lionel Hampton and Benny Carter playing themselves. In 1949, Hawks reteamed with Grant in the screwball comedy I Was a Male War Bride, also starring Ann Sheridan.

In 1951, Hawks produced, and according to some, directed, a science-fiction film, The Thing from Another World. Director John Carpenter stated: "And let's get the record straight. The movie was directed by Howard Hawks. Verifiably directed by Howard Hawks. He let his editor, Christian Nyby, take credit. But the kind of feeling between the male characters—the camaraderie, the group of men that has to fight off the evil—it's all pure Hawksian." He followed this with the 1952 Western The Big Sky, starring Kirk Douglas. Later in 1952, Hawks worked with Grant for the fifth and final time in the screwball comedy Monkey Business, which also starred Marilyn Monroe and Ginger Rogers. Grant plays a scientist (reminiscent of his character in Bringing up Baby) who creates a formula that increases his vitality. Film critic John Belton called the film Hawks's "most organic comedy". Hawks's third film of 1952 was a contribution to the omnibus film O. Henry's Full House, which includes short stories by the writer O. Henry made by various directors. Hawks's short film The Ransom of Red Chief starred Fred Allen, Oscar Levant and Jeanne Crain.

In 1953, Hawks made Gentlemen Prefer Blondes, which famously featured Marilyn Monroe singing " Diamonds Are a Girl's Best Friend ". The film starred Monroe and Jane Russell as two cabaret performing best friends; many critics argue that the film is the only female version of the "buddy film" genre. Choreographer Jack Cole is generally credited with staging the musical numbers while Hawks is credited with directing the non-musical scenes. In 1955, Hawks made Land of the Pharaohs, a sword-and-sandal epic about ancient Egypt that stars Jack Hawkins and Joan Collins. The film was Hawks's final collaboration with longtime friend William Faulkner. In 1959, Hawks worked with John Wayne in Rio Bravo, also starring Dean Martin, Ricky Nelson and Walter Brennan as four lawmen "defending the fort" of their local jail in which a local criminal is awaiting a trial while his family attempt to break him out. The screenplay was written by Furthman and Leigh Brackett, who had collaborated with Hawks previously on The Big Sleep. Film critic Robin Wood has said that if he "were asked to choose a film that would justify the existence of Hollywood... it would be Rio Bravo."

In 1962, Hawks made Hatari!, again with Wayne, who plays a wild animal catcher in Africa. It was also written by Leigh Brackett. Hawks's knowledge of mechanics allowed him to build the camera-car hybrid that allowed him to film the hunting scenes in the film. In 1964, Hawks made his final comedy, Man's Favorite Sport?, starring Rock Hudson (since Cary Grant felt he was too old for the role) and Paula Prentiss. Hawks then returned to his childhood passion for car races with Red Line 7000 in 1965, featuring a young James Caan in his first leading role. Hawks's final two films were both Western remakes of Rio Bravo starring John Wayne and written by Leigh Brackett. In 1966, Hawks directed El Dorado, starring Wayne, Robert Mitchum, and Caan, which was released the following year. He then made Rio Lobo, with Wayne in 1970. After Rio Lobo, Hawks planned a project relating to Ernest Hemingway and "Now, Mr. Gus", a comedy about two male friends seeking oil and money. He died in December 1977, before these projects were completed.