In 1918 Tate entered Vanderbilt University in Nashville, Tennessee, where he helped found The Fugitive (1922–25), a magazine for a group of young poets known as the Fugitives (Fugitive). Tate introduced the Fugitives to the poetry of T.S. Eliot (Eliot, T.S.), whose attitudes toward modern life and whose emphasis on the hollowness of modern man found an echo in Tate's own themes. Tate contributed to the symposium I'll Take My Stand (1930), a manifesto defending the traditional agrarian society of the South.

From 1934 Tate taught at Southwestern College in Memphis, Tennessee, the Woman's College of the University of North Carolina, Princeton University, and the University of Minnesota (1951–68). In 1943 he was named poetry consultant to the Library of Congress. He held the position, which later became known as the poet laureate consultant in poetry of the United States, for one year. Tate then joined The Sewanee Review, which acquired wide importance as a literary magazine under his editorship (1944–46).

In Tate's best-known poem, “Ode to the Confederate Dead” (first version, 1926; rev. 1930), the dead symbolize the emotions that the poet is no longer able to feel. The poems written from about 1930 to 1939 broadened this theme of disjointedness by showing its effect on society, as in the sadly ironic “The Mediterranean” (1932). In his later poems Tate suggested that only through the subjective wholeness of the individual can society itself be whole. This view emerged tentatively in “Seasons of the Soul” (1943) and confidently in “The Buried Lake” (1953), both devotional poems.

Tate's only novel, The Fathers (1938), refashioned the Jason-Medea myth to promulgate agrarian beliefs. His Collected Poems was published in 1977; Essays of Four Decades appeared in 1969.