Tate was born near Winchester, Kentucky to John Orley Tate, a businessman, and Eleanor Parke Custis Varnell. In 1916 and 1917 Tate studied the violin at the Cincinnati Conservatory of Music.

He began attending Vanderbilt University in 1918, where he met fellow poet Robert Penn Warren. Warren and Tate were invited to join a group of young Southern poets under the leadership of John Crowe Ransom; the group were known as the Fugitive Poets and later as the Southern Agrarians. Tate contributed to the group's magazine The Fugitive and to the agrarian manifesto I'll Take My Stand published in 1930. Tate also joined Ransom to teach at Kenyon College in Gambier, Ohio.

In 1924, Tate moved to New York City where he met poet Hart Crane, with whom he had been exchanging correspondence for some time. During a summer visit with Warren in Kentucky, he began a relationship with writer Caroline Gordon. They married in New York in May 1925. Their daughter Nancy was born in September.

He and Gordon were divorced in 1945 and remarried in 1946. Though devoted to one another for life, they could not get along and later divorced again.

In 1950, Tate converted to Roman Catholicism.

Tate married the poet Isabella Gardner in the early fifties. While teaching at the University of Minnesota in Minneapolis, he met Helen Heinz, a nun enrolled in one of his courses, and began an affair with her. Gardner divorced Tate.

He married Heinz in 1966. They moved to Sewanee, Tennessee. In 1967 Tate became the father of twin sons, John and Michael. Michael died at eleven months from choking on a toy. A third son Benjamin was born in 1969.

In 1924, Tate began a four-year sojourn in New York City where he worked freelance for The Nation, contributed to the Hound and Horn, Poetry magazine, and others. He worked as a janitor, and lived la vie boheme in Greenwich Village with Caroline Gordon, and when urban life proved too overwhelming, repaired to "Robber Rocks", a house in Patterson, New York, with friends Slater Brown and his wife Sue, Hart Crane, and Malcolm Cowley. He would, some years later, contribute to the conservative National Review as well.

1928 saw the publication of Tate's most famous poem, "Ode to the Confederate Dead", not to be confused with "Ode to the Confederate Dead at Magnolia Cemetery" written by American Civil War poet and South Carolina native, Henry Timrod. In 1928, Tate also published a biography Stonewall Jackson: The Good Soldier.

In 1929, Tate published a second biography Jefferson Davis: His Rise and Fall.

By the 1930s, Tate had returned to Tennessee, where he worked on social commentary influenced by his agrarian philosophy. In addition to his work on I'll Take My Stand, he published Who Owns America?, which was a conservative response to Franklin D. Roosevelt's New Deal. During this time, Tate also became the de facto associate editor of The American Review, which was published and edited by Seward Collins. Tate believed The American Review could popularize the work of the Southern Agrarians. He objected to Collins's open support of Fascists Benito Mussolini and Adolf Hitler, and condemned fascism in an article in The New Republic in 1936.

In 1938 Tate published his only novel, The Fathers, which drew upon knowledge of his mother's ancestral home and family in Fairfax County, Virginia.

Tate was a poet-in-residence at Princeton University until 1942. He founded the Creative Writing program at Princeton, and mentored Richard Blackmur, John Berryman, and others. In 1942, Tate assisted novelist and friend Andrew Lytle in transforming The Sewanee Review, America's oldest literary quarterly, from a modest journal into one of the most prestigious in the nation. Tate and Lytle had attended Vanderbilt together prior to collaborating at The University of the South.

Tate died in Nashville, Tennessee. His papers are collected at the Firestone Library at Princeton University.

Poetry

• Poems, 1928-1931, 1932.
• The Mediterranean and Other Poems, 1936.
• Selected Poems, 1937.
• The Winter Sea, 1944.
• Poems, 1920-1945, 1947.
• Poems, 1922-1947, 1948.
• Two Conceits for the Eye to Sing, If Possible, 1950.
• Poems, 1960.
• Poems, 1961.
• Collected Poems, 1970.
• The Swimmers and Other Selected Poems, 1970.

Prose

• Stonewall Jackson: The Good Soldier, 1928.
• Jefferson Davis: His Rise and Fall, 1929.
• Robert E. Lee, 1932.
• Reactionary Essays on Poetry and Ideas, 1936.
• The Fathers, 1938.
• Reason in Madness, 1941.
• On the Limits of Poetry: Selected Essays, 1928-1948, 1948.
• The Hovering Fly, 1949.
• The Forlorn Demon, 1953.
• The Man of Letters in the Modern World, 1955.
• Collected Essays, 1959.
• Essays of Four Decades, 1969.
• Memoirs and Opinions, 1926-1974, 1975.