He coached Jackson State University from 1953 to 1962, where he compiled a record of 63–37–5. Merritt led Jackson State to back-to-back appearances in the Orange Blossom Classic in 1961 and 1962 before being hired by what was then Tennessee A&I. At Tennessee State (as Tennessee A&I was renamed in 1968), Merritt had four undefeated seasons, claimed four Midwest Athletic Association titles, seven black college football national championships: (1965, 1966, 1970, 1971, 1973, 1979 and 1982) and earned the school's first-ever NCAA Division I-AA playoff victory in 1982.
John Merritt Boulevard in Nashville, Tennessee is named in his honor. The Tennessee State football team usually opens every home season with the John Merritt Classic game at Nissan Stadium, traditionally against Alabama A&M University, but more recently the game has also headlined other from other universities.
