On the opera stage Chookasian returned to the Spoleto Festival in 1962 to sing Clarissa in Prokofiev's "The Love for Three Oranges". In 1963 she made her first of several appearances at the New York City Opera in the title role of Menotti's "The Medium". She made her first appearance at the Bayreuth festival in 1965 singing in three of her Wagner roles: Mary, the First Norn, and Erda. In 1966 she made her first appearances with the Opéra de Montréal and the American Opera Society. In 1970 she made her debut with the San Francisco Opera as Mistress Quickly. In 1973 she sang Amneris at the Palacio de Bellas Artes in Mexico City and sang Erda in "Siegfried" for her debut with the Lyric Opera of Chicago. In 1976 she notably sang in the world premiere of Thomas Pasatieri's "Inés de Castro" and sang Ulrica with the Philadelphia Lyric Opera Company. She also appeared with the Zurich Opera, the Salzburg Festival, the New Orleans Opera, the Houston Grand Opera, and other companies in the United States and Europe. Chookasian would often bring her husband with her when she traveled as his work in real estate was flexible enough for him to travel. Chookasian fondly recounted one of her most memorable trips to Yerevan, Armenia in a 1997 "Opera News" interview. Chookasian was invited to the city to perform in two productions mounted in her honor: Amneris in "Aida" and the Armenian composer Tigran Chukhajian's opera "Arshak II".