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Ashley became made his first recordings with Garley Foster and Doc Walsh in 1928. Throughout the late 20s and early 30s, Ashley recorded with Gwen Foster, The Blue Ridge Mountain Entertainers and Byrd Moore & His Hot Shots. He also made solo banjo recordings. He would become well known for his recordings of "The Coo-Coo Bird," "The House Carpenter" and "Peg and Awl" (Carolina Tar Heels) which were featured on Harry Smith's Anthology of American Folk Music. For several of his solo songs Ashley used a G-modal banjo tuning that he called the 'sawmill' tuning (gDGCD).

In the folk music revival of the late 1950s and early 1960s, urban ethnomusicologists rediscovered Ashley's music. In 1960 Ralph Rinzler met Ashley at the Old Time Fiddler's Convention in Union Grove, NC. He eventually persuaded him to start playing banjo again and to record his repertoire of songs. Over the next few years he and his friends, including Doc Watson, played at many urban folk festivals. They also made two records for the Folkways label. While Ashley was an accomplished guitar player as well as banjo player, after being rediscovered, he only played banjo.