Ashton studied dancing in London under Léonide Massine, Nicholas Legat, and Marie Rambert, who encouraged his first choreographic efforts, The Tragedy of Fashion (1926) and Capriol Suite (1930).

Ashton joined the Vic-Wells (later the Sadler's Wells and then the Royal) Ballet in 1933 and distinguished himself as a mime and character dancer in such roles as Carabosse in The Sleeping Beauty and the gigolo in Façade and as the versatile choreographer of ballets that include Cinderella, Sylvia, and Daphnis and Chloë and the film Tales of Hoffmann (1951). He was the Royal Ballet's principal choreographer from 1933 to 1970, during which time he also served as its associate director (1952 to 1963) and its director (1963 to 1970). In 1970 he retired from his administrative position in order to devote his time exclusively to choreography.

In 1963 Ashton created Marguerite and Armand especially for the new partnership of Margot Fonteyn and Rudolf Nureyev. Others included The Dream (1964), a one-act ballet based on Shakespeare's A Midsummer Night's Dream; Monotones (Part I, 1965; Part II, 1966), to music of Erik Satie; Jazz Calendar (1968); Enigma Variations (1968); A Month in the Country (1976); and Rhapsody (1981), based on music by Sergey Rachmaninoff. In 1970 Ashton choreographed and danced in the motion picture Tales of Beatrix Potter. His major works include such enduring favourites as Façade (1931), Les Rendezvous (1933), Les Patineurs (1937), Symphonic Variations (1946), Illuminations (for the New York City Ballet, 1950), Homage to the Queen (1953), Romeo and Juliet (for the Royal Danish Ballet, 1955), Birthday Offering (1956), Ondine (1958), and La Fille mal gardée (1960). Ashton was knighted in 1962.