The globally successful invasive snail, Potamopyrgus antipodarum (Tateidae), is rarely parasitized except in its native New Zealand where it is infected as first intermediate host by at least 20 species of trematode parasitic castrators. In France and Poland, only one trematode parasitic castrator, belonging to the Aporocotylidae (the blood flukes of fishes), is known to infect P. antipodarum, and its origin remains a mystery. We investigated the genetic identities, taxonomic relationships, and prevalences of this parasite and other aporocotylids infecting P. antipodarum and closely related snails in a French stream, and throughout New Zealand and southeast Australia. ITS2 DNA sequences of the French parasite matched with Aporocotylid sp. I (sensu Hechinger, 2012) from P. antipodarum in New Zealand. Hence, the aporocotylid parasite in Europe most likely originated from the native range of the introduced host. Aporocotylid sp. I was rare in both native and invasive ranges, infecting overall less than 1 out of 1,000 snails. The parasite and its host have a persistent relationship in France, as they both were repeatedly encountered over a period of 14 years. Our molecular phylogeny also reveals that this parasite is part of a diverse and poorly known group of aporocotylids in New Zealand and southeastern Australia.