An original member of the Jazz Messengers, he later played in Horace Silver's quintet and freelanced with Gene Ammons, Kenny Burrell, Donald Byrd, Art Farmer, Jackie McLean, Hank Mobley, Lee Morgan, Sonny Rollins, and Phil Woods among others.
Some of Watkins' best-known work can be heard when as a 22-year-old he appeared on the 1956 album, Saxophone Colossus by tenor saxophonistSonny Rollins, with Max Roach and Tommy Flanagan. From that session, the tunes "Blue Seven" and "St. Thomas," especially, have become revered not only as evidence of Rollins' original genius but as fine examples of Watkins' work.
According to Horace Silver's autobiography, Let's Get to the Nitty Gritty, Watkins, along with Silver, later left Art Blakey's Jazz Messengers because the other members of the band at the time (Kenny Dorham, Hank Mobley and Blakey) had serious drug problems, whereas Watkins and Silver were tired of being harassed and searched by the police every time they went to a gig in a new city and club.
In 1958 Watkins would join Donald Byrd for a European tour, taking up extended residence at Le Chat Qui Pêche, a jazz club on Paris' Left Bank. Along with Byrd, tenor saxophonist Bobby Jaspar, pianist Walter Davis, Jr. and drummer Art Taylor, Watkins made two albums with Byrd during this time, one recorded in the club and another at a formal concert featuring Byrd's quintet.
Watkins was known for his superb tone and distinct phrasing. He had a distinct walking tone and was right on the beat, forming an organic, indivisible relationship with his instrument as he swayed with it in perfect time. Pianist Red Garland often stated that Watkins was his favorite bassist and that he was always in tune and never off-key. Watkins played with Garland in 1959, along with drummer Specs Wright.
While Watkins lived only to the age of 27, he appeared on well over 350 LPs in his career backing many major jazz stars of the time. When Charles Mingus briefly ventured over to the piano stool in 1961, he hired Watkins to take over the bass part; Oh Yeah!!! and Tonight at Noon were the results of this adventurous interlude.