Born in Dublin, Duff first played competitive Gaelic football during his schooling. He later joined the Fingallians club and won a county junior championship medal in 1993.
Duff made his debut on the inter-county scene at the age of seventeen when he was picked on the Dublin minor team. He won a Leinster medal in this grade in 1979. Duff later joined the Dublin under-21 team, winning a Leinster medal in 1980. By this stage he had joined the Dublin senior team, making his debut during the 1979-80 league. Over the course of the next thirteen seasons Duff won one All-Ireland medal in 1983. He also won four Leinster medals, two National Football League medals and two All-Stars. He retired from inter-county football during the 1991-92 league.