Host behavioural modification by parasites is a common and well-documented phenomenon. However, knowledge on the complexity and specificity of the underlying mechanisms is limited, and host specificity among manipulating parasites has rarely been experimentally verified. We tested the hypothesis that the ability to infect and manipulate host behaviour is restricted to phylogenetically closely related hosts. Our model system consisted of the brain-encysting trematode Euhaplorchis sp. A and six potential fish intermediate hosts from the Order Cyprinodontiformes. Five co-occurring cyprinids were examined for naturally acquired brain infections. Then we selected three species representing three levels of taxonomic relatedness to a known host to experimentally evaluate their susceptibility to infection, and the effect of infection status on behaviours presumably linked to increased trophic transmission. We found natural brain infections of Euhaplorchis sp. A metacercariae in three cyprinids in the shallow sublittoral zone. Of the three experimentally exposed species, Fundulus grandis and Poecilia latipinna acquired infections and displayed an elevated number of conspicuous behaviours in comparison with uninfected controls. Euhaplorchis sp. A was able to infect and manipulate fish belonging to two different families, suggesting that ecological similarity rather than genetic relatedness determines host range in this species.