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Many parasite species use multiple host species to complete development; however, empirical tests of models that seek to understand factors impacting evolutionary changes or maintenance of host number in parasite life cycles are scarce. Specifically, Brown et al.’s (2001) mating system model, which posits multi-host life cycles are an adaptation to prevent inbreeding in hermaphroditic parasites and thus, preclude inbreeding depression, remains untested. The model assumes loss of a host results in parasite inbreeding and predicts host loss can only evolve if there is no parasite inbreeding depression. We provide the first empirical tests of this model using a novel approach we developed for assessing inbreeding depression from field-collected, parasite samples. The method compares genetically-based, selfing-rate estimates to a demographic-based selfing rate, which was derived from the closed mating system experienced by endoparasites. Results from the hermaphroditic trematode Alloglossidium renale, which has a derived 2-host life cycle, supported both the assumption and prediction of the mating system model as this highly inbred species had no indication of inbreeding depression. Additionally, comparisons of genetic and demographic selfing rates revealed a mixed mating system that could be explained completely by the parasite’s demography, i.e., its infection intensities.