Non-native species have the potential to alter host community structure, which, in turn, may affect parasite transmission, diversity and distribution, particularly when the introduced host is ecologically or phylogenetically related to its native host(s). In this study, we examine whether the introduction of a competent non-native fish host shifts parasite load and community composition in native fish species. Specifically, we focus on two Eupercarian species: the native Eurasian perch (Perca fluviatilis) and the non-native pumpkinseed sunfish (Lepomis gibbosus), which was introduced into Europe from North America. Our results show that the parasite community of native perch co-occurring with non-native pumpkinseed (sympatric populations) differ significantly from those of perch inhabiting sites unaffected by pumpkinseed introduction (allopatric populations). Moreover, sympatric perch populations exhibit significantly higher parasite abundance, infracommunity richness and dominance, along with lower equitability, compared to allopatric populations. These findings suggest that the introduction of pumpkinseed may have contributed to shifts in both parasite abundance and diversity in native fish hosts. Additionally, our study indicates a potential parasite spillback of the trematode Bucephalus polymorphus and spill-over of the Asian invasive parasitic copepod Neoergasilus japonicus, both associated with pumpkinseed establishment in the study area. The successful inclusion of non-native fish species into the life cycles of several independently introduced and unrelated invasive parasites underscores the importance of introduced hosts in driving changes within local parasite communities.