Dandridge was born in Cleveland, Ohio to Cyril Dandridge (October 25, 1895-July 9, 1989), a cabinetmaker and minister and Ruby Dandridge (née Butler), an aspiring entertainer. Dandridge's parents separated shortly before her birth. Ruby Dandridge soon created an act for her two young daughters, Vivian and Dorothy, under the name of "The Wonder Children." The daughters toured the Southern United States for five years while Ruby worked and performed in Cleveland. During this time, they toured non-stop and rarely attended school.
With the start of the Great Depression, work dried up, as it did for many of the Chitlin' circuit performers. Ruby Dandridge moved to Hollywood, where she found steady work playing domestics in small parts on radio and film. "The Wonder Kids" were renamed "The Dandridge Sisters" and booked into such venues as the Cotton Club and The Apollo Theater in Harlem, New York. Dandridge's first on-screen appearance was a bit part in a 1935 Our Gang short. In 1937 she appeared in the Marx Brothers feature A Day at the Races.
In 1940, Dandridge played a murderer in the race film Four Shall Die. All of her early parts were stereotypical African-American roles, but her singing ability and presence brought her popularity in nightclubs around the country. During this period, she starred in several "soundies", film clips designed to be displayed on juke boxes, including "Paper Doll" by the Mills Brothers, "Cow Cow Boogie", "Jig in the Jungle", "Mr. & Mrs. Carpenter's Rent Party."
In 1954, director and writer Otto Preminger cast Dandridge, along with Harry Belafonte, Pearl Bailey, Brock Peters, Diahann Carroll, Madame Sul-Te-Wan (uncredited), and Joe Adams in his production of Carmen Jones. Dandridge's singing voice was dubbed by Marilyn Horne.
Carmen Jones grossed $60,000 during the first week and $47,000 in the second upon release in 1955. The film received favorable reviews, and Dandridge was nominated for an Academy Award for Best Actress, becoming only the third African American to receive a nomination in any Academy Award category (after Hattie McDaniel and Ethel Waters). Grace Kelly won for her performance in The Country Girl. At the ceremony, Dandridge presented the Academy Award for Film Editing to Gene Milford for On the Waterfront.
Dandridge married dancer and entertainer Harold Nicholas on September 6, 1942, and gave birth to her only child, Harolyn Suzanne Nicholas, on September 2, 1943. Harolyn was born brain-damaged, and the couple divorced in October 1951.
Dandridge married Jack Denison on June 22, 1959, although amid allegations of domestic abuse and financial setbacks, the pair was divorced. At this time, Dandridge discovered that the people who were handling her finances had swindled her out of $150,000, and that she was $139,000 in debt for back taxes. Forced to sell her Hollywood home and to place her daughter in a state mental institution in Camarillo, California, Dandridge moved into a small apartment at 8495 Fountain Avenue in West Hollywood, California. Alone and without any acting roles or singing engagements on the horizon, Dandridge suffered a nervous breakdown. Shortly thereafter, Earl Mills started arranging her comeback.
On September 8, 1965, Dandridge spoke with friend Gerry Branton. Dandridge was scheduled to fly to New York the next day to prepare for her nightclub engagement at Basin Street East. Several hours after her conversation with Branton ended, Dandridge was found dead by her manager, Earl Mills. Two months later a Los Angeles pathology institute determined the cause to be an accidental overdose of Imipramine, a tricyclic antidepressant. She was 42 years old.
On September 12, 1965, a private funeral service was held for Dandridge at the Little Chapel of the Flowers; then she was cremated and her ashes were entombed in the Freedom Mausoleum at Forest Lawn Cemetery in Glendale, California.
For her contribution to the motion picture industry, Dorothy Dandridge has a star on the Hollywood Walk of Fame at 6719 Hollywood Boulevard.