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In 1908, Griffith accepted a role as a stage extra in Professional Jealousy for the American Mutoscope and Biograph Company, where he met cameraman Billy Bitzer, and his career in the film industry changed forever. In 1908, Biograph's main director Wallace McCutcheon Sr. grew ill, and his son Wallace McCutcheon Jr. took his place. McCutcheon Jr. did not bring the studio success; Biograph co-founder Harry Marvin then gave Griffith the position, and he made the short The Adventures of Dollie. He directed a total of 48 shorts for the company that year.
Among the films he directed in 1909 was The Cricket on the Hearth, an adaptation of Charles Dickens' novel. On the influence of Dickens on his own film narrative, Griffith employed the technique of cross-cutting—where two stories run alongside each other, as seen in Dickens' novels such as Oliver Twist. When criticized by a cameraman for doing this in a later film, Griffith was said to have replied, "Well, doesn't Dickens write that way?".
His short In Old California (1910) was the first film shot in Hollywood, California. Four years later, he produced and directed his first feature film Judith of Bethulia (1914), one of the earliest films to be produced in the U.S. Biograph believed that longer features were not viable at this point. According to Lillian Gish, the company thought that "a movie that long would hurt [the audience's] eyes".
Griffith left Biograph because of company resistance to his goals and his cost overruns on the film. He took his company of actors with him and joined the Mutual Film Corporation. There he co-produced The Life of General Villa, a silent biographical-action movie starring Pancho Villa as himself, shot on location in Mexico during a civil war. He formed a studio with Majestic Studios manager Harry Aitken, which became known as Reliance-Majestic Studios and later was renamed Fine Arts Studios. His new production company became an autonomous production unit partner in the Triangle Film Corporation along with Thomas H. Ince and Keystone Studios' Mack Sennett. The Triangle Film Corporation was headed by Aitken, who was released from the Mutual Film Corporation, and his brother Roy.
Griffith directed and produced The Clansman through Reliance-Majestic Studios in 1915. The film later became known as The Birth of a Nation. It is one of the early feature length American films. The film was a success, but it aroused much controversy due to its depiction of slavery, the Ku Klux Klan, and race relations in the American Civil War and the reconstruction era of the United States. It was based on Thomas Dixon Jr.'s 1905 novel The Clansman: A Historical Romance of the Ku Klux Klan; it depicts Southern slavery as benign, the enfranchisement of freedmen as a corrupt plot by the Republican Party, and the Ku Klux Klan as a band of heroes restoring the rightful order. This view of the era was popular at the time and was endorsed for decades by historians of the Dunning School, although it met with strong criticism from the National Association for the Advancement of Colored People (NAACP) and other groups.
The NAACP attempted to stop showings of the film. This was successful in some cities, but nonetheless it was shown widely and became the most successful box-office attraction of its time. It is considered among the first "blockbuster" motion pictures, and it broke all box-office records that had been established until then. "They lost track of the money it made", Lillian Gish remarked in a Kevin Brownlow interview.
Audiences in some major northern cities rioted over the film's racial content and the violence. Griffith's indignation at efforts to censor or ban the film motivated him the following year to produce Intolerance, in which he portrayed the effects of intolerance in four different historical periods: the Fall of Babylon; the Crucifixion of Jesus; the events surrounding the St. Bartholomew's Day massacre (during religious persecution of French Huguenots); and a modern story. Intolerance was not a financial success; it did not bring in enough profits to cover the lavish road show that accompanied it. Griffith put a huge budget into the film's production that could not be recovered in its box office. He mostly financed Intolerance himself, which contributed to his financial ruin for the rest of his life.
Griffith's production partnership was dissolved in 1917, and he went to Artcraft, part of Paramount Pictures, and then to First National Pictures (1919–1920). At the same time, he founded United Artists together with Charlie Chaplin, Mary Pickford, and Douglas Fairbanks; the studio was premised on allowing actors to control their own interests rather than being dependent upon commercial studios.
He continued to make films, but he never again achieved box-office grosses as high as either The Birth of a Nation or Intolerance.
Later film career
Though United Artists survived as a company, Griffith's association with it was short lived. While some of his later films did well at the box office, commercial success often eluded him. Griffith features from this period include Broken Blossoms (1919), Way Down East (1920), Orphans of the Storm (1921), Dream Street (1921), One Exciting Night (1922), and America (1924). Of these, the first three were successes at the box office. Griffith was forced to leave United Artists after Isn't Life Wonderful (1924) failed at the box office.
He made a part talkie, Lady of the Pavements (1929), and only two full-sound films: Abraham Lincoln (1930) and The Struggle (1931). Neither was successful, and after The Struggle he never made another film.
In 1936, director Woody Van Dyke, who had worked as Griffith's apprentice on Intolerance, asked Griffith to help him shoot the famous earthquake sequence for San Francisco, but Griffith was not given any film credit. Starring Clark Gable, Jeanette MacDonald and Spencer Tracy, it was the top-grossing film of the year.
In 1939, the producer Hal Roach hired Griffith to produce Of Mice and Men (1939) and One Million B.C. (1940). He wrote to Griffith: "I need help from the production side to select the proper writers, cast, et cetera, and to help me generally in the supervision of these pictures."
Although Griffith eventually disagreed with Roach over the production and departed, Roach later insisted that some of the scenes in the completed film were directed by Griffith. This would make the film the final production in which Griffith was actively involved. However, cast members' accounts recall Griffith directing only the screen tests and costume tests. When Roach advertised the film in late 1939 with Griffith listed as producer, Griffith asked that his name be removed.
Griffith was for decades held in awe by many members of the film industry. He was presented a special Oscar by the Academy of Motion Picture Arts and Sciences in the mid 1930s. In 1946, he made an impromptu visit to the film location of David O. Selznick's epic western Duel in the Sun, where some of his veteran actors—Lillian Gish, Lionel Barrymore and Harry Carey—were cast members. Gish and Barrymore found their old mentor's presence distracting and became self-conscious; in response, Griffith hid behind the scenery when the two were filming their scenes.