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Cukor graduated from the DeWitt Clinton High School in 1917 and was enrolled at the City College of New York. He lost interest in his studies and dropped out before taking a job as an assistant stage manager and bit player for a touring production of the British musical "The Better 'Ole".

In the 1920's Cukor stage managed the Knickerbocker Players before becming the general manager of the Lyceum Players and eventually co-founding the C.F. and Z. Production Company. With this theatrical company, Cukor started working as a theatrical director and made his Broadway directorial debut with the play "Antonia".

The C.F. and Z. Production Company was eventually renamed the Cukor-Kondolf Stock Company, and started recruiting up-and-coming theatrical talents including Louis Calhern, Ilka Chase, Bette Davis, Douglass Montgomery, Frank Morgan, Reginald Owen, Elizabeth Patterson, and Phyllis Povah.

Cukor attained great critical acclaim in 1926 for directing "The Great Gatsby", an adaptation of the novel by F. Scott Fitzgerald and directed six more Broadway productions until 1929. At that time Cukor was hired by Paramount Pictures and started as an apprentice director before the studio lent him to Universal Pictures. His first notable film work was serving as a dialogue director for "All Quiet on the Western Front" (1930).

After returning to Paramount Pictures, he worked as a co-director until his first solo directorial effort on "Tarnished Lady" (1931), and co-directed "One Hour with You" (1932) with Ernst Lubitsch, but was only given a credit as assistant director. He left Paramount in protest, moving to RKO Studios.

During the 1930s, Cukor  worked frequently with Katharine Hepburn though not always with box-office success.

In 1936, Cukor was assigned to work on the film adaptation of "Gone with the Wind" spending two years on the film's pre-production, supervising screen tests for actresses seeking to play leading character Scarlett O'Hara. Cukor favored casting either Katharine Hepburn or Paulette Goddard but producer David O. Selznick refused to cast either, since Hepburn was viewed as "box office poison," while Goddard was rumored to have had a scandalous affair with Charlie Chaplin.

Cukor did not get to direct "Gone with the Wind", his involvement limited to coaching actresses Vivien Leigh and Olivia de Havilland. Similarly, the very same year, Cukor also failed to receive a directing credit for "The Wizard of Oz" (1939), though he was responsible for several casting and costuming decisions.

In this same period, Cukor did direct an all-female cast in "The Women" (1939), as well as Greta Garbo's final motion picture performance in "Two-Faced Woman" (1941). His film career was interrupted when he joined the Signal Corps in 1942. Given his experience, Cukor was soon assigned to producing training and instructional films for army personnel. He wanted to gain an officer's commission, but was denied promotion above the rank of private. Cukor suspected that rumors of his homosexuality were the reason he never received the promotion.

During the 1940s, Cukor had a number of box-office hits, such "A Woman's Face" (1941) and "Gaslight" (1944). He forged a working alliance with screenwriters Garson Kanin and Ruth Gordon, and the trio collaborated on seven films between 1947-1954.

Until the early 1950s, most of Cukor's films were in black-and-white, and his first film in Technicolor was "A Star Is Born" (1954), with Judy Garland as the leading actress. Casting the male lead for the film proved difficult, as several major stars were either not interested in the role or were considered unsuitable by the studio. Cukor had to settle for James Mason as the male lead, but the film was highly successful and received 6 Academy Award nominations. But Cukor was not nominated for directing.

He had a handful of critical successes over the following years, such as Les Girls (1957) and "Wild Is the Wind" (1957), and also helmed the unfinished "Something's Got to Give" (1962), which had a troubled production and went at least $2 million over budget before it was terminated.

Cukor had a comeback with the critically and commercially successful "My Fair Lady," one of the highlights of his career, for which he won both an Academy Award. a Golden Globe and a Directors Guild of America Award. However, his career very quickly slowed.

Cukor's most notable film in the 1970s was the fantasy The Blue Bird (1976) , which was the first joint Soviet-American production. It was a box-office flop, though it received a nomination for the Saturn Award for Best Fantasy Film and was groundbreaking for its time. Cukor's swan song was "Rich and Famous" (1981), depicting the relationship of two women over a period of several decades., played by co-stars Jacqueline Bisset and Candice Bergen, Cukor's final pair of leading ladies.

He retired as a director at the age of 82, and died a year later of a heart attack. He was buried at the Forest Lawn Memorial Park in Glendale, next to his long-time friend Frances Howard, the wife of legendary studio mogul Samuel Goldwyn.