Hairston was born in Belews Creek, a rural community on the border of Stokes and Forsyth counties in North Carolina. At an early age he and his family moved to Pittsburgh, Pennsylvania. His grandparents had been slaves.
He graduated cum laude from Tufts University and studied music at the Juilliard School as well. He worked as a choir conductor in the early stages of his career. His work with choirs on Broadway eventually led to his singing and acting in plays, films, radio programs, and television shows.
In his later years, Hairston served as a cultural ambassador for American music, traveling to numerous countries with choral groups that he had assembled. In 1985 he took the Jester Hairston Chorale, a multi-racial group, to sing in China, at a time when foreign visitors were still quite rare in that country.