Stokes' father, Durham Stokes, was a multi-millionaire stock broker who had once stood for Parliament as aLiberal Partycandidate. His affluence allowed the younger Stokes to live financially independent his entire life. Adrian Stokes attendedRugby School. During World War I his elder brother Philip was killed in France. Stokes entered Magdalen College, Oxford where he read philosophy, politics and classics. He achieved a second class in those fields in 1923 as well as excellence in tennis. After graduation, Stokes travelled to India and returned by way of China and the United States. It was these travels, as well as a college visit to Italy, that fostered an appreciation of art as the means to make sense of life.
His first book, published in 1925, The Thread of Ariadne, was based on that thesis. The same year he moved to Venice to write and research on the Italian renaissance. Two events in the late 1920s would change his life and art-historical writings profoundly. In 1926, Stokes met Ezra Pound at Rapallo, Italy. In 1929 he began therapy with the Freudian psychoanalyst Melanie Klein (1882–1960) to investigate his bisexuality and depression. Pound's literary conception of the Italian renaissance and Klein's psychoanalytic theory would figure strongly in Stoke's art history. His essays in The Criterion magazine began to be published in collected works. Pound prevailed upon T. S. Eliot (then editor at Faber & Faber) to publish the first two of Stokes' books of art history essays, The Quattro Cento: A Different Conception of the Italian Renaissance, 1932, and The Stones of Rimini, 1934. That same year Stokes moved to England to live among the British artists at Parkhill Road, Hampstead, painting and writing reviews for the Spectator. In 1937 he studied painting at the Euston Road School with William Coldstream (1908–1987), Lawrence Gowing, F. Graham Bell (1910–1943) and Victor Pasmore (1908–1998). His book Form and Colour of the same year displays the sensibilities of an artist as much as an art historian. In 1938 he married the Scottish painter Margaret Mellis (b. 1914). The couple moved to Carbis Bay, Cornwall, shortly before World War II, joining other artists from London, including Barbara Hepworth, Ben Nicholson, Naum Gabo and Peter Lanyon, a native of Cornwall (1918–1964). After stormy years of marriage and the birth of a son, Telfer (1940), Stokes divorced only to marry his ex-wife's sister, Ann Mellis (b. 1922), in 1947 requiring a move to Ticino, Switzerland, with more liberal laws of consanguinity. A second son was born in 1948. Stokes returned to England in 1950 to Hurtwood House, Guildford. Many of the paintings for which he is known today were produced during this time.
Together with his friend Ben Nicholson, he contributed to the second number of Polemic (No. 2, January 1946), a short-lived British "Magazine of Philosophy, Psychology, and Aesthetics".
His post-war writing included two autobiographical works, Inside Out, 1947, and Smooth and Rough, 1951. Longer essays on individual artists such as Cézanne, 1947, Raphael, 1956 and Monet, 1958 also appeared. These works continued to use Freudian analysis as a basis to explain art. A major work of his later years using psychological interpretation, Michelangelo: A Study in the Nature of Art, appeared in 1955. His most programmatic use of psychology as a tool for the art historian appeared in 1963 as Painting and the Inner World, including an interview with the psychiatrist Donald Meltzer.
From 1960–67 Stokes was a trustee of the Tate Gallery, London. In 1967, his final work Reflections on the Nude was both a synthesis of his ideas as well as the conclusion of his writing on art. Diagnosed with a brain tumor in 1971, he focused on his painting until his death the following year. His paintings are owned by a number of galleries including the Tate. A retrospective exhibition was held at the Serpentine Gallery, London, in 1982. A collection of poems, With All the Views, appeared in London in 1981.
Stokes was completely self-educated in art history. His wealth allowed him to consort with the intelligentsia of Europe, travelling with the Sitwells, tennis with Ezra Pound, sharing a villa with Aldous Huxley in Sanary. It also freed him from constraints of writing to please mainstream art-historical audiences. Marginalized by the emerging Warburg art historians whom he disputed on aesthetic and psycho-analytical grounds, Stokes was championed in the 1950s after a period of neglect by his friends Richard Wollheim (1923–2003) and the critics Andrew Forge and David Sylvester. Methodologically, Stokes continues the British aesthetic-school art writing of John Ruskin and Walter Pater, reacting against the formalism of the Bloomsbury group. Later art historians such as John Berger, Peter Fuller, Michael Baxandall, John Shearman and John Gage owe a debt to Stokes' "phenomenological precision" (Read).