Born into an African-American family of devout Seventh-day Adventists in New Orleans, Louisiana, Verrett showed early musical abilities, but initially a singing career was frowned upon by her family. Later Verrett went on to study in Los Angeles, California and at the Julliard School in New York.

In 1957, Verrett made Her operatic debut in Britten's Lucretia. In 1958, she made her New York City Opera as Irina in Kurt Weill’s Lost in the Stars. In 1959, she made her European debut in Cologne in Nabokov's Rasputins Tod. In 1962, she received critical acclaim for her Carmen in Spoleto, and repeated the role at the Bolshoi Theatre in 1963, the NY City Opera in 1964, and La Scala in 1966. In 1968, she made her debut at the Metropolitan Opera in 1968, also with Carmen. Verrett first appeared at the Royal Opera House, Covent Garden in 1973. Verrett's roles included Dido, Leonora in La Favorita, Gluck's Orpheus, Amneris, and Selika in L'africaine.

Beginning in the late 1970s she began to tackle soprano roles, including Tosca, Norma, Lady Macbeth, and Aida. In 1990, Verrett sang Dido Les Troyens at the inauguration of the Opera Bastille in Paris.

In 2003, Verrett published a memoir, I Never Walked Alone (ISBN 0471209910) in which she spoke frankly about the racism she encountered as a black person in classical music world of the United States. When the conductor Leopold Stokowski invited her to sing with the Houston Symphony in the early 1960s, he had to rescind his invitation when the orchestra board refused to accept a black soloist. Stokowski later made amends by giving her a prestigious date with the much better known Philadelphia Orchestra.