Born Constance Halverstadt in Seattle, Washington to Dallas Halverstadt and Kate Cummings, she began as a stage actress, landing her first Broadway show by the age of eighteen. While appearing on Broadway, she was discovered by Sam Goldwyn, who brought her to Hollywood in 1931.

Between 1931 and 1934, Cummings appeared in 21 films, most notably the Harold Lloyd picture Movie Crazy, and American Madness, which was directed by Frank Capra. She was married to the then screenwriter Benn W. Levy (March 7, 1900 - December 7, 1973) from July 3, 1933 until his death. Levy went on to write and direct films for Cummmings, such as The Jealous God (1939); he ended his career as the Labour MP for Eton and Slough. They had a son and a daughter.

Cummings was uncomfortable in Hollywood and moved to England, where she continued acting, both in movies and on the stage. Few of these films became popular in America, although included amongst those that did is Blithe Spirit, adapted from a play by Sir Noel Coward.

In 1974, Cummings, who resided in the UK for many decades, was made a Commander of the British Empire for her contributions to the British entertainment industry. There is no record of her relinquishing her USA citizenship, and unless she had acquired dual British and American citizenship, the award would have been honorary. It was reported in the Sunday Times (December 22, 2003) that in 1975 she was offered a life peerage, but declined it. (see ). A peerage would have been possible only if she had acquired British citizenship.

In 1979, she won a Tony Award for Best Actress, recognising the strength of her performance in the role of Emily Stilson (a former aviator who has a hemorrhagic stroke, from which she struggles to recover) in the play Wings by Arthur Kopit.

She was a committee member of the Royal Court Theatre and the Arts Council. She has a star on the Hollywood Walk of Fame at 6211 Hollywood Blvd.