Childhood was one of the major themes of Jarrell's verse, and he wrote about his own extensively in The Lost World (1965). With an M.A. from Vanderbilt University (1938), he began his career as a teacher. His first book of verse, Blood for a Stranger, was published in 1942, the same year he joined the U.S. Army Air Forces. Many of his best poems appeared in Little Friend, Little Friend (1945) and Losses (1948), both of which dwell on war-based themes.

Jarrell taught at Sarah Lawrence College in Bronxville, New York (1946–47), and his only novel, the sharply satirical Pictures from an Institution (1954), is about a similar progressive women's college. He was a teacher at the University of North Carolina at Greensboro from 1947 until his death in a road accident, which may or may not have been a suicide, and from 1956 to 1958 he served as poetry consultant to the Library of Congress (now poet laureate consultant in poetry). He was widely considered the shrewdest literary critic of his day.

Jarrell's criticism has been collected in Poetry and the Age (1953), A Sad Heart at the Supermarket (1962), and The Third Book of Criticism (1969). Jarrell's later poetry—The Seven-League Crutches (1951), The Woman at the Washington Zoo (1960), and The Lost World—restored an openness to emotion (some called it sentimentality) rarely found in works of “academic” poets of the period. His Complete Poems appeared in 1969, and a selection of his critical essays, No Other Book, was published in 2000.