Ashbery was born in Rochester, New York and raised on a farm near Lake Ontario; his brother died when they were children. Ashbery was educated at the Deerfield Academy. At Deerfield, Ashbery read such poets as W. H. Auden, Dylan Thomas, and Wallace Stevens, and began writing poetry; one of his poems was actually published in Poetry Magazine, though under the name of a classmate who had submitted it without Ashbery's knowledge or permission. His first ambition was to be a painter. From the age of eleven until fifteen he took weekly classes at the art museum in Rochester.


He was graduated from Harvard College (A.B. 1949, cum laude), where he was a member of the Harvard Advocate, the university's literary magazine, and the Signet Society. He wrote his senior thesis on the poetry of W.H. Auden. At Harvard he befriended fellow writers Kenneth Koch, Barbara Epstein, V.R. Lang, Frank O'Hara, and Edward Gorey, and was a classmate of Robert Creeley, Robert Bly, and Peter Davison. Ashbery went on to study briefly at New York University, and received a M.A. from Columbia in 1951.

From the mid-1950s, when he received a Fulbright Fellowship, through 1965, he lived in France. He served as the art editor for the European edition of the New York Herald Tribune, while also translating potboilers and contemporary French literature. During this period he lived with the French poet Pierre Martory. After returning to the United States, he continued his career as an art critic, for New York and Newsweek magazines, while also serving on the editorial board of ARTNews until 1972. Several years later, he began a stint as an editor at Partisan Review, serving from 1976 to 1980.

In the early 1970s, Ashbery began teaching at Brooklyn College, where his students included poet John Yau, and in the 1980s, he moved to Bard College, where he is the Charles P. Stevenson, Jr., Professor of Languages and Literature. He was the poet laureate of New York state from 2001 to 2003, and also served for many years as a chancellor of the Academy of American Poets.

Ashbery's long list of awards began with the Yale Younger Poets Prize in 1956, selected by W. H. Auden, for his first collection, Some Trees. His early work shows the influence of W. H. Auden, Wallace Stevens, Boris Pasternak, and many of the French surrealists (his translations from French literature are numerous). In the late 1950s, the critic John Bernard Myers categorized the common traits of Ashbery's avant-garde poetry, as well as that of Kenneth Koch, Frank O'Hara, James Schuyler, Barbara Guest, Kenward Elmslie and others, as constituting a "New York School." Ashbery then wrote two collections while in France, the highly controversial The Tennis-Court Oath (1962), and Rivers and Mountains (1966), before returning to New York to write The Double-Dream of Spring, which was published in 1970.

Increasing critical recognition in the 1970s transformed Ashbery from an obscure avant-garde experimentalist into one of America's most important (though also still most controversial) poets. After the publication of Three Poems (1973), Ashbery in 1975 picked up all three major American poetry prizes (the Pulitzer Prize, the National Book Award, and the National Book Critics Circle Award) for his Self-Portrait in a Convex Mirror. The collection's title poem is considered to be one of the masterpieces of late 20th century American poetic literature.

His subsequent collection, the more difficult Houseboat Days (1977) reinforced Ashbery's reputation as did As We Know in 1979, which contains the long, double-columned poem "A Litany." By the 1980s and 1990s, Ashbery had become a central figure in American and more broadly English-language poetry, as a number of imitators evidenced. His own poetry was accused of a staleness in this period, but books like A Wave (1985) and the later And the Stars Were Shining (1994), particularly in their long poems, show an unmistakably original and great poet in practice.

Ashbery's works are characterized by a free-flowing, often disjunctive syntax, extensive linguistic play, often infused with considerable humor, and a prosaic, sometimes disarmingly flat or parodic tone. The play of the human mind is the subject of a great many of his poems. Formally the earliest poems show the influence of conventional poetic practice, yet by the Tennis Court Oath a much more revolutionary engagement with form, and formlessness, is on display. Ashbery returned to something approximating conventional verse, at least on its surface, with many of the poems in The Double Dream of Spring, though his Three Poems are written in long blocks of prose. Although he has never approached the radical experimentation of The Tennis Court Oath poems or "The Skaters" and "Into the Dusk-Charged Air" from his collection Rivers and Mountains, his syntactic and semantic experimentation, linguistic expressiveness and deft, often abrupt shifting of registers, and insistent wit remain consistent elements of his work.

Ashbery art criticism has been collected in the 1989 volume Reported Sightings, Art Chronicles 1957-1987, edited by the poet David Bergman. He has written one novel, A Nest of Ninnies, with fellow poet James Schuyler, and in his 20s and 30s penned several plays, which have been collected in Three Plays (1978). Ashbery's Charles Eliot Norton Lectures at Harvard University were published as "Other Traditions" in 2000. A larger collection of his prose writings, Selected Prose, appeared in 2005.

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