Host resistance to parasites is a rapidly evolving trait that can influence how hosts modify ecosystems. Eco-evolutionary feedbacks may develop if the ecosystem effects of host resistance influence selection on subsequent host generations. In a mesocosm experiment, using a recently diverged (<100 generations) pair of lake and stream three-spined sticklebacks, we tested how experimental exposure to a common fish parasite (Gyrodactylus spp.) affects interactions between hosts and their ecosystems in two environmental conditions (low and high nutrients). In both environments, we found that stream sticklebacks were more resistant to Gyrodactylus and had different gene expression profiles than lake sticklebacks. This differential infection led to contrasting effects of sticklebacks on a broad range of ecosystem properties, including zooplankton community structure and nutrient cycling. These ecosystem modifications affected the survival, body condition, and gene expression profiles of a subsequent fish generation. In particular, lake juvenile fish suffered increased mortality in ecosystems previously modified by lake adults, whereas stream fish showed decreased body condition in stream fish-modified ecosystems. Parasites reinforced selection against lake juveniles in lake fish-modified ecosystems, but only under oligotrophic conditions. Overall, our results highlight the overlapping timescales and the interplay of host–parasite and host–ecosystem interactions. We provide experimental evidence that parasites influence host-mediated effects on ecosystems and, thereby, change the likelihood and strength of eco-evolutionary feedbacks.