With H.G. Wells, George Bernard Shaw and others, Asquith founded London's Film Society in 1925, and after a filmmaking apprenticeship in Hollywood, returned to England as a director in 1928. Along with Alfred Hitchcock, he was considered a major force in the British cinema during the 1930s and 40s. Beginning with his directing debut, "Shooting Stars" (co-directed with A.V. Bramble; 1928) which utilized experimental visual effects and "A Cottage on Dartmoor" (1929), a portrait of British life notable for its use of sound, Asquith became recognized for his tasteful, restrained and civilized quasi-documentary portraits of British life and manners.

With his superb film version of Shaw's "Pygmalion" (1938; co-directed with Leslie Howard), Asquith also began turning out expertly crafted theatrical adaptations, one of the finest of which is the delicious "The Importance of Being Earnest" (1952). From 1938 he began a profitable collaboration with playwright-screenwriter Terrence Rattigan, creating emotional studies of people under stress including, perhaps their finest joint work, "The Way to the Stars" (1945) as well as "The Winslow Boy" (1948), and "The Browning Version" (1950), and continuing through Asquith's last film, "The Yellow Rolls Royce" (1964). Son of liberal prime minister Lord Herbert Asquith.