In Chicago, Wolf hired the guitarist Jody Williams, but in 1954 he invited Sumlin to move to Chicago to play the second guitar in his band. Williams left the band in 1955, leaving Sumlin as the primary guitarist, a position he held almost continuously (except for a brief spell playing with Muddy Waters around 1956) for the remainder of Wolf’s career. According to Sumlin, Howlin’ Wolf sent him to a classical guitar instructor at the Chicago Conservatory of Music to learn keyboards and scales. Sumlin played on the album Howlin’ Wolf (called the “rocking chair album”, with reference to its cover illustration), which was named the third greatest guitar album of all time by Mojo magazine in 2004.

Upon Wolf’s death in 1976, Sumlin continued playing with several other members of Wolf’s band, as the Wolf Gang, until about 1980. He also recorded under his own name, beginning with a session from a tour of Europe with Wolf in 1964. His last solo album was About Them Shoes, released in 2004 by Tone-Cool Records. He underwent lung removal surgery the same year, but he continued performing until just before his death. His final recording, just days before his death, was tracks for an album by Stephen Dale Petit, Cracking The Code (333 Records).