Multi-host parasites can exploit various host species that differ in abundance and susceptibility to infection, which will contribute unequally to their transmission and fitness. Several species of acanthocephalan manipulative parasites (among which Pomphorhynchus laevis and P. tereticollis) use various amphipod species of the genus Gammarus as intermediate hosts. Many Gammarus pulex and G. fossarum cryptic lineages are living in sympatry in European rivers, questioning the spectrum of intermediate hosts that acanthocephalans can use, and their relative contribution to their life cycles. In this work, the respective roles of parasites species (P. laevis and, for the first time, P. tereticollis) and sympatric host cryptic species (within the complex G. pulex/fossarum) were studied experimentally on two traits: host susceptibility to infection and parasite virulence. Differences were found, both in terms of infectivity and virulence, between the cryptic hosts and between the two parasite species. We confirm that these acanthocephalans, previously considered as generalists, show specificities among their sympatric hosts. If G. pulex was more susceptible to P. laevis than G. fossarum, differences in susceptibility to P. tereticollis were more pronounced among cryptic species within the G. fossarum species complex than between G. pulex and G. fossarum. The mortality of infected individuals increased significantly after several weeks of development in both parasite species. P. tereticollis was less virulent than P. laevis, perhaps in link with differences in host exploitation, since we evidenced that P. tereticollis had a much slower growth rate.