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 Deerfield Academy. At Deerfield, an all-boys school, Ashbery read such poets as W. H. Auden and Dylan Thomas, and began writing poetry. One of his poems was published in Poetry magazine, although under the name of a classmate who had submitted it without Ashbery's knowledge or permission. He also published a handful of poems, including a sonnet about his frustrated love for a fellow student, and a piece of short fiction in the school newspaper, the Deerfield Scroll. 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.Ashbery graduated in 1949 with an A.B., cum laude, from Harvard College, 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 an M.A. from Columbia in 1951.

After working as a copywriter in New York from 1951 to 1955, from the mid-1950s, when he received a Fulbright Fellowship, through 1965, Ashbery lived in France. He was an editor of the twelve issues of Art and Literature (1961-64) and the New Poetry special issue of Harry Mathews' Locus Solus magazine (# 3/4; 1962). To make ends meet he translated french murder mysteries, he served as the art editor for the European edition of the New York Herald Tribune and was an art critic for Art International (1960-65) and Paris correspondent (1963-66) for Art News, when Thomas Hess took over as editor. During this period he lived with the French poet Pierre Martory, whose books Every Question but One (1990), The Landscape Is behind the door (1994) and The Landscapist he has translated (2008), as he has Jean Perrault (Camouflage), Max Jacob (The Dice Cup), Pierre Reverdy and Raymond Roussel. 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.

During the fall of 1963, Ashbery became acquainted with Andy Warhol at a scheduled poetry reading at the Literary Theatre in New York. He had also previously written favorable reviews of Warhol's art. That same year he reviewed Warhol's Flowers exhibition at Galerie Illeana Sonnabend in Paris, describing Warhol's visit to Paris as "the biggest transatlantic fuss since Oscar Wilde brought culture to Buffalo in the nineties." Ashbery returned to New York near the end of 1965 and was welcomed with a large party at the Factory. He became close friends with poet Gerard Malanga, Warhol's assistant, on whom he had an important influence as a poet.

In the early 1970s, Ashbery began teaching at Brooklyn College, where his students included poet John Yau. In the 1980s, he moved to Bard College, where he was the Charles P. Stevenson, Jr., Professor of Languages and Literature, until 2008, when he retired; since that time, he has continued to win awards, present readings, and work with graduate and undergraduates at many other institutions. 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. He serves on the contributing editorial board of the literary journal Conjunctions. He was a Millet Writing Fellow at Wesleyan University, in 2010, and participated in Wesleyan's Distinguished Writers Series. Ashbery lives in New York City and Hudson, New York, with his partner, David Kermani.

Ashbery's long list of awards began with the Yale Younger Poets Prize in 1956. The selection, by W. H. Auden, of Ashbery's first collection, Some Trees, later caused some controversy. 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 still one of its most controversial) poets. After the publication of Three Poems (1973), Ashbery in 1975 won 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 1979's As We Know, which contains the long, double-columned poem "Litany." By the 1980s and 1990s, Ashbery had become a central figure in American and more broadly English-language poetry, as his 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 the unmistakable originality of a 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. Ashbery once said that his goal was "to produce a poem that the critic cannot even talk about." Formally, the earliest poems show the influence of conventional poetic practice, yet by The Tennis Court Oath a much more revolutionary engagement with form appears. 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 again 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, syntactic and semantic experimentation, linguistic expressiveness, deft, often abrupt shifts of register, and insistent wit remain consistent elements of his work.

Ashbery's 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, three of 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 and his poetry volume Where shall I wander? appeared in 2005. In 2008, his Collected Poems 1956—1987 was published as part of the Library of America series.

The Oxonian Review summarised his work 2009:

This past October, the Library of America released John Ashbery’s Collected Poems (1956—1987), making him the first living poet to be “canonised” in the series. It is a fitting honour for a man whose decades-long reign as one of the high priests of the contemporary American poetry scene has always been something of a paradox. Having received nearly every major award for achievement in the humanities, he continues to incite considerable debate as to whether his poems “mean” anything at all. To read an Ashbery poem with the intent to explicate in the traditional sense is to make a daring, perhaps foolhardy, leap of semantic faith.

• Turandot and Other Poems (1953)
• Some Trees (1956), winner of the Yale Younger Poets Prize that year
• The Tennis Court Oath (1962)
• Rivers and Mountains (1966)
• The Double Dream of Spring (1970)
• Three Poems (1972)
• The Vermont Notebook (1975)
• Self-Portrait in a Convex Mirror (1975), awarded the Pulitzer Prize, the National Book Award, and the National Book Critics Circle Award
• Houseboat Days (1977)
• As We Know (1979)
• Shadow Train (1981)
• A Wave (1984), awarded the Lenore Marshall Poetry Prize and the Bollingen Prize by Yale University
• April Galleons (1987)
• The Ice Storm (1987)
• Flow Chart (1991)
• Hotel Lautréamont (1992)
• And the Stars Were Shining (1994)

• Can You Hear, Bird? (1995)
• The Mooring of Starting Out: The First Five Books of Poetry (Ecco) collection of the poet's work from 1956 to 1972; a New York Times "notable book of the year" (1998)
• Wakefulness (1998)
• Girls on the Run (1999), a book-length poem inspired by the work of artist/novelist Henry Darger
• Your Name Here (2000)
• 100 Multiple-Choice Questions (2000)
• Other Traditions, 6 long essays on 6 other poets (2000) Harvard University Press
• As Umbrellas Follow Rain (2001)
• Chinese Whispers (2002)
• Selected Prose 1953-2003 (2005)
• Where Shall I Wander (2005) (finalist for the National Book Award)
• A Worldly Country (2007)
• Notes from the Air: Selected Later Poems (2007) (winner of the 2008 International Griffin Poetry Prize)
• Martory, Pierre The Landscapist Ashbery (Tr.) Carcanet Press (2008)
• Planisphere (2009)