During his club career, Di Gennaro played for Fiorentina (1976–80), Perugia (1980–81), Hellas Verona (1981–88) and Bari (1988–91). He made his professional debut with his hometown club Fiorentina at the age of 18, although, despite his talent, he struggled to find space in the club due to the presence of the team's star playmaker Giancarlo Antognoni, with whom Di Gennaro faced competition for a starting spot as the two did not play well alongside each other. As a result, he moved to Perugia during the 1980–81 season, in order to gain more playing time, although it proved to be a negative season, as Perugia were ultimately relegated to Serie B at the end of the campaign. Di Gennaro switched clubs once again the following season, joining Verona; whilst at the club, he became a key player, serving as the team's main playmaker in midfield. He helped lead the club from Serie B to Serie A in his first season, and was also a member of the side that won the club's first ever Serie A title during the 1984–85 season, under manager Osvaldo Bagnoli; in total, Di Gennaro made 182 appearances for Verona, scoring 18 goals. He later joined Bari in 1988, where he served as the team's captain, helping the team to obtain promotion to Serie A and winning the Mitropa Cup in 1990, before retiring in 1991, after helping the club avoid relegation.