Parasites can negatively affect hosts at individual, population, and species‐level scales. However, the link between individual‐ and population‐level impacts is often poorly understood. In particular, the population‐level response to parasitism may alter wider ecosystem dynamics if animals with ecosystem engineering capabilities are infected. Here, we examine the effects of parasitism on a freshwater ecosystem engineer, the unionid mussel Anodonta anatina, at two different sites. We study three common parasites: the digenean trematode Rhipidocotyle campanula; the unionicolid mite Unionicola intermedia; and the ectoparasitic invasive zebra mussel Dreissena polymorpha. As well as demonstrating the individual‐level effects of parasitism on the native host mussel, we construct a simple model to estimate the reduction in population‐level reproductive output caused by parasites. We show that both infection prevalence and intensity were population‐specific, with one site having more than three times as many native mussels infected by trematodes and mites than the other, but more than four times fewer mussels afflicted by invasive zebra mussels. Negative reproductive consequences for individual host mussels were documented as a result of parasitism, with trematodes causing castration at both sites. Mites were also correlated with a reduction in the viability of larval offspring (glochidia) by more than 25%, but only at one site, suggesting some potential impacts of parasitism may be population specific. The population‐level model shows that parasitism alone reduces larval output of the two populations by 10% and 13%, respectively. Our study takes the important step of scaling individual‐level effects of parasitism to population‐level processes, and highlights the influence that parasites may have in the population dynamics of unionid mussels. Given the ecosystem engineering capabilities of A. anatina, such effects may have important impacts on the wider biota. Even at relatively low prevalences, the observed effects of parasites on native mussel populations suggests that parasitism must be considered in the conservation of freshwater mussels, one of the world's most globally imperilled faunal groups. Further, understanding how the effects of parasitism on individual hosts scales to the ecosystem level is a crucial and unaddressed question in freshwater biology.