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John Collins' first music teacher was his mother, jazz pianist Georgia Gorham, who worked as a sheet music demonstrator for W.C. Handy and later led her own small band. At fourteen, John was touring with his mother's unit. Seven years later, he was with Art Tatum, and the music world was becoming acutely aware of the brilliant young Alabama-born guitarist.
Collins went on to play with Lester Young, Benny Carter, Fletcher Henderson, Dizzy Gillespie but his most famous role was as a vital element in the famed Nat "King" Cole sound from 1951-1965.
On September 15, 1985, Mayor Tom Bradley proclaimed John Collins Day in Los Angeles, California, and the Los Angeles Jazz Society declared The Year of the Guitar in recognition of Collin's artistic excellence and inspiration to generations of musicians. In 1983 the Jazz Heritage Foundation presented a plaque to Collins for "Forty Years of contributions to the History of Jazz." In 1980, the Smithsonian Institution at Washington, D.C. honored him for "Outstanding Contributions to the Oral History of Jazz."
In 1993, Collins was inducted into the Alabama Jazz Hall of Fame in Birmingham, Alabama.