In 1955, she won two California state competitions sponsored by the Young Musicians Foundation, and later that year she appeared on Talent Scouts, a national television show hosted by Arthur Godfrey.

In 1962, she received critical acclaim for portraying Bizet's Carmen at the Festival dei Due Mondi in Spoleto; she repeated the role at the Bolshoi Theatre in 1963, and at the New York City Opera in 1964 (opposite Richard Cassilly and Norman Treigle).

Beginning in the late 1970s, Verrett began to tackle soprano roles, including Selika in L'Africaine, Judith in Bartók's Bluebeard's Castle, Lady Macbeth in Macbeth, Madame Lidoine in Poulenc's Dialogues of the Carmelites (Met 1977), Tosca, Norma (from Boston 1976 till Messina 1989), Aida (Boston 1980 and 1989), Desdemona (Otello) (1981), Leonore (Fidelio, Met 1983), Iphigénie (1984–85), Alceste (1985), and Médée (Luigi Cherubini) (1986).

In December 1978, Verrett sang the role of Tosca in a Live from the Met television broadcast opposite Luciano Pavarotti as Cavaradossi and Cornell MacNeil as Scarpia.

[10] In 1990, Verrett sang Didon in Les Troyens at the inauguration of the Opéra Bastille in Paris, and added a new role to her repertoire: Santuzza in Mascagni's Cavalleria rusticana, in Siena.

In 1994, she made her Broadway debut in the Tony Award-winning revival of Rodgers and Hammerstein's Carousel at Lincoln Center's Vivian Beaumont Theater, playing Nettie Fowler.

The preceding year, at the National Opera Association Gala Banquet and Concert honoring Mattiwilda Dobbs, Todd Duncan, Camilla Williams, and Robert McFerrin, Verrett said: I'm always so happy when I can speak to young people because I remember those who were kind to me that didn't need to be.

[15] In 2003, Shirley Verrett published a memoir, I Never Walked Alone (ISBN 978-0-471-20991-1), in which she spoke frankly about the racism she encountered as a black person in the American classical music world.