A recent epidemic of the invasive monogenean Neoheterobothrium hirame is suspected to have caused the significant decline of the commercial catch of olive flounder, Paralichthys olivaceus, in Japan. To clarify the causal link between parasite invasion and host depletion, we monitored the infections of N. hirame on juvenile flounder for 2 years at two widely separate bays, Obama Bay, experiencing a devastating reduction in flounder catches, and Miyako Bay with a stable catch. Prevalence, mean intensity and abundance of developmental stages of N. hirame were compared between the bays and between fish year classes. Fishes captured at Obama Bay harboured three times more worms than those at Miyako Bay and had a significantly higher overall prevalence of infection. In addition, there was a negative correlation between parasite intensity and host condition factor at Obama Bay, suggesting a causal link between the N. hirame epidemic and the reduction of local flounder populations.