James Ingram Merrill was born in New York City on March 3, 1926, and grew up in Manhattan and Southampton. He was the son of Charles Merrill, co-founder of the brokerage firm Merrill Lynch, and his second wife, Hellen Ingram. He began writing poems as a child, and at age sixteen, while he was in prep school, his father had a book of them privately printed under the title Jim's Books.

Merrill's studies at Amherst College were interrupted by service in the U.S. Army from 1944 to 1945. Another book, The Black Swan, was privately printed in 1946 while he was still in college. Following his graduation in 1947, he taught for a year at Bard College. His first trade book, First Poems, was published by Alfred A. Knopf in 1951 to critical acclaim. In 1956 he used a portion of his inheritance to found the Ingram Merrill Foundation, which has since awarded grants to hundreds of artists and writers. Over the next decade he published two novels, The Seraglio (1957) and The (Diblos) Notebook (1965) as well as two books of poems, The Country of a Thousand Years of Peace (1959) and Water Street (1962). His 1966 collection of poems, Nights and Days, won the National Book Award and brought his work a wider audience.

He went on to earn numerous awards for his poetry, including the Bollingen Prize for Braving the Elements (1972), the Pulitzer Prize for Divine Comedies (1976), and a second National Book Award for Mirabell (1978). In 1983, his epic poem The Changing Light at Sandover (1982) won the National Book Critics Circle Award.

On February 6, 1995 James Merrill died of a heart attack in Tucson, Arizona. His last book, A Scattering of Salts, was published a month later.