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Parasitism is a potential mechanism initiating or facilitating ecotypic differentiation and speciation in freshwater fish. While recent studies have begun to explore this question, there are no empirical studies of parasitism in evolutionary replicates of ecotype-pairs at variable stages of speciation. Such comparative studies of parasitism along continuums of host differentiation are needed as a first step towards testing the role of parasites in ecological speciation. We explored parasitism of whitefish Coregonus lavaretus in four pre-alpine lakes in Switzerland that hold replicate species radiations of whitefish. We sampled shallow and deep-spawning ecotypes on their breeding grounds. We found significant and consistent differences in infection between the ecotypes so that the shallow-spawning fish had more trematode infections, whereas the deepspawning fish had more cestodes. The magnitude of these differences correlated positively with the degree of the genetic differentiation among the ecotypes and negatively with the extent of eutrophication of the lakes. Although the overall diversity of infections was low, some parasite species with potential effects on fish showed marked differences in infection between the ecotypes, suggesting that parasitism may have a role in maintaining ecotype differentiation in this system. Our results also indicate previously unknown habitat segregation of the better differentiated ecotypes, i.e. species, along the depth gradient outside the breeding season. Moreover, oligotrophic lakes tended to have higher parasite species richness and higher abundances of infection, than mesotrophic and eutrophic lakes, suggesting that the history of eutrophication affects parasite diversity.