Transmission rate between hosts is a major determinant of fitness in parasites with complex life cycles and this has favoured the development of sophisticated adaptations in parasites to increase the probability of transmission. On the other hand, increasing pressure by parasites has forced the target hosts to develop means to control or prevent the infections. This study examined the transmission of the trematode parasite Diplostomum spathaceum between the two intermediate hosts, the freshwater snail (Lymnaea stagnalis) and rainbow trout (Oncorhynchus mykiss), focusing on the parasite strategies in cercarial production from the snail host in laboratory conditions and responses of the fish host to cercarial infection. Infected snails released cercariae for an extended period of time in accordance with the bet hedging hypothesis, which suggests spreading the risk of transmission failure in an environment with an unpredictable host contact probability. Bet hedging was not found in association with cercarial quality, but cercariae were released in higher numbers during day compared to night. High prevalence and intensity of infection in wild fish populations suggests that the parasite strategies are likely to maintain effective transmission to fish. As a response against the cataract-causing parasite, fish hosts acquired physiological resistance, which decreased the number of establishing parasites although the resistance proved to be insufficient to prevent cataract formation. However, this study demonstrated for the first time that the fish also decreased exposure to the parasite by avoiding the cercariae. Thus, a combination of resistance and avoidance behaviour may provide more efficient defence against the parasite. Individual differences between fish in exposure to the parasite and ability to avoid cercariae probably cause the parasites to aggregate in a few host individuals, which has important implications for the parasite population dynamics and transmission. As a practical application, the results of this study allow the estimation of key parameters in the parasite transmission dynamics, which can be used in designing preventative methods against D. spathaceum outbreaks in fish farming industry.