The maintenance of strict host specificity by parasites when several closely related host species live in sympatry is poorly understood. Species of intertidal trochid snails in the genera Diloma, Melagraphia and Austrocochlea often occur together and are parasitised by a single digenean morphotype (Platyhelminthes, Trematoda), tentatively placed in Opecoelidae. Of the 10 trochid species (6 from New Zealand, 4 from Australia) we examined, six were found to be infected, and the prevalence of infection was as high as 17.5%. We obtained molecular data (mitochondrial 16S and nuclear rDNA internal transcriber spacer 2 sequences, representing 774 bp), to infer phylogenetic relationships amongst these Digenea. Our phylogeny separated the single morphotype into three clearly defined clades (which are almost certainly separate biological species): (i) those infecting two species of Austrocochlea from Tasmania, (ii) those infecting Diloma subrostrata in Otago and Southland, New Zealand, and (iii) those infecting all the parasitised New Zealand topshells (Melagraphia aethiops, D. subrostrata, Diloma nigerrima and Diloma arida) throughout the country. This last group comprised two subclades, one infecting only D. subrostrata and one infecting the other three species. Two D. subrostrata populations were each found to be infected by genetically distinct parasites, yet sympatric populations of the other snails were not necessarily infected. This study is thus the first to reveal cryptic species of digeneans in a single population of a molluscan first intermediate host. We point out also that the degree of host specificity would have been grossly underestimated if, in the absence of our genetic analysis, we had only considered digenean morphology. Our results shed light on the conditions that may favour switching among intermediate hosts in digeneans, and on the presence/absence of host specificity in these parasites.