Parasites of the genus Hepatocystis are close relatives of Plasmodium that frequently infect epauletted fruit bats across West and East Africa. Our understanding of susceptible hosts and prevalence of infection of Hepatocystis remains fragmented. Non-invasive sampling of bat assemblages in representative habitats critically contribute to haemosporidian parasite distribution maps. Here, we report on a survey of Hepatocystis parasite infections in bats undertaken over two consecutive years in a protected area in Nigeria, where prevalence and diversity of bat-infecting haemosporidian parasites have not been studied. Microscopic examination of blood films in combination with PCR detection and sequencing revealed Hepatocystis infections with prevalences of 25% and 42% in the closely related epauletted fruit bats Epomophorus sp. and Micropteropus pusillus. For the first time, mature Hepatocystis gametocytes were identified in one Egyptian fruit bat (Rousettus aegyptiacus). This novel host record was confirmed by parasite and host genotyping and suggests that Hepatocystis parasites have a broader host distribution in African fruit bats than currently known.