Beginning on trombone at age seven, Teagarden was entirely self-taught. After drifting across the Southwest, he eventually arrived in New York City in 1927 and made his recording debut; from that moment he was the acknowledged master of his idiom. He led his own band (1939–47), played with Louis Armstrong (1947–51), and re-formed his band (1951–57); although he never achieved commercial success, he retained his full powers until the end of his life. His movies include Birth of the Blues (1941). His style was remarkable for its effortless flow of melodic ideas, technical poise, and the tender beauty of its overall effect. He was also an outstanding jazz singer. His voice, with an engaging Southern drawl, ranged somewhere between the rasp of Louis Armstrong and the smooth sound of Bing Crosby, with whom he was professionally associated from time to time.

Jack's brother, Charlie Teagarden, played trumpet off and on in Jack's bands and did free-lance work for several well-known bandleaders, including Paul Whiteman, Jimmy and Tommy Dorsey, and Bob Crosby.