Multi-host helminth systems are difficult to study at a population level due to inherent spatial and temporal sampling challenges. Consequently, our understanding of the factors affecting gene flow, genetic drift and effective population size is limited. Population genetic parameters (Ne, Θ, π) are necessary in understanding fundamental processes in host-parasite evolution such as co-evolutionary dynamics, spread of resistance alleles and local adaptation. This study used museum specimens collected over 20-years of three congeneric trematode (Schistosomatidae) species: Trichobilharzia querquedulae, T. physellae, and Trichobilharzia species A . All contribute to the worldwide zoonotic disease cercarial dermatitis (i.e. swimmers Itch). Populations of each species were sampled for two mitochondrial (cox1 and nad4) and one nuclear loci (ITS1) to estimate population genetic structure, genetic diversity, effective size and population history. Significant differences in these measures were revealed among the three congeners. Trichobilharzia querquedulae maintained a well-connected globally diverse metapopulation, with an effective size approximately three times that of the other two species, which were characterized by lower overall genetic diversity and greater population structure, mediated by the definitive duck host. We hypothesize that the species-specific patterns are due to distinctive ecological preferences and migratory behaviors of their respective definitive hosts. This study demonstrates the value of natural history collections to facilitate population genetic studies that would otherwise be infeasible. Applying population genetic data within this comparative congeneric framework allows us to tease apart particular aspects of host-parasite natural history and its influence on microevolutionary patterns within complex helminth systems, including contributions to zoonotic disease.