Because he was nearsighted and slight of stature, he was often ostracized by his peers. In response, Hayden read voraciously, developing both an ear and an eye for transformative qualities in literature. He attended Detroit City College later called Wayne State University with a major in Spanish and minor in English, and left in 1936 during the Great Depression, one credit short of finishing his degree, to go to work for the Works Progress Administration Federal Writers’ Project, where he researched black history and folk culture.

Leaving the Federal Writers’ Project in 1938, Hayden married Erma Morris in 1940 and published his first volume, Heart-Shape in the Dust (1940). He enrolled at the University of Michigan in 1941 and won a Hopwood Award there. Raised as a Baptist, he followed his wife into the Baháʼí Faith during the early 1940s, and raised a daughter, Maia, in the religion. Hayden became one of the best-known Baháʼí poets. Erma Hayden was a pianist and composer and served as supervisor of music for Nashville public schools.

In pursuit of a master’s degree, Hayden studied under W. H. Auden, who directed his attention to issues of poetic form, technique, and artistic discipline. Auden’s influence may be seen in the “technical pith of Hayden’s verse”. After finishing his degree in 1942, then teaching several years at Michigan, Hayden went to Fisk University in 1946, where he remained for twenty-three years, returning to Michigan in 1969 to complete his teaching career.

On April 7, 1966, Hayden’s Ballad of Remembrance was awarded, by unanimous vote, the Grand Prize for Poetry at the first World Festival of Negro Arts in Dakar, Senegal. The festival had more than ten thousand people from thirty-seven nations in attendance. However, on April 22, 1966, Hayden was denounced at a Fisk University conference of black writers by a group of young protest poets led by Melvin Tolson for refusing to identify himself as a black poet.

Hayden was elected to the American Academy of Poets in 1975. His most famous poem is “Those Winter Sundays”, which deals with the memory of fatherly love and loneliness. It ranks among the most anthologized American poems of the twentieth century. He declined the position later called United States Poet Laureate previously, accepted the appointment for 1976–1977 during America’s Bicentennial, and again in 1977–1978 though his health was failing then. He was awarded successive honorary degrees by Brown University (1976) and Fisk, (1978). In 1977 he was interviewed for television in Los Angeles on At One With by Keith Berwick. In January 1980 Hayden was among those gathered to be honored by President Jimmy Carter and his wife at a White House reception celebrating American poetry. He served for a decade as an editor of the Baháʼí journal World Order.

He died in Ann Arbor, Michigan, on February 25, 1980, age 66.

In 2012 the U.S. Postal Service issued a pane of stamps featuring ten great Twentieth Century American Poets, including Hayden.