The effect of waterborne zinc (Zn) on Gyrodactylus population dynamics was studied on isolated guppies maintained at concentrations ranging from 0 to 240 μg Zn/l. After 1 week pre-exposure to Zn, each fish was experimentally infected with 3 gyrodactylids and parasite numbers were recorded daily on each fish until the fish either died or recovered from infection. Parasite establishment was most successful at 0 and 240 μg Zn/l (97%) compared with the intermediate Zn concentrations. Low to moderate concentrations of Zn were beneficial to the parasite, as evidenced by the concentration-dependent increase in peak parasite burden on recovered fish up to 120 μg Zn/l. In contrast, 240 μg Zn/l may have been toxic to the parasite, as both peak parasite burden (in fish that recovered from infection), and maximum rate of increase of the parasite population (in fish that died) declined at this concentration. The combined effect of infection and Zn is harmful to the fish, because mortality of infected fish (but not uninfected fish) increased with increasing Zn concentrations. We suggest that the observed mortality occurs because of the inability of fish to continuously produce mucous that is a key factor for protecting fish from both waterborne Zn and ectoparasites.