Phylogenetic inference of Hepatocystis, a haemosporidian parasite of diverse primate and bat hosts, revealed that the parasites from Australasian Pteropus bat species form a distinct clade to all other Hepatocystis parasites from Africa and Asia. Here, we investigate the phylogenetic placement of Hepatocystis in the Australian bat Pteropus poliocephalus for the first time and examine parasite morphology and prevalence from selected points across its range. Hepatocystis infections were detected in low prevalences in P. poliocephalus in contrast to high numbers in P. alecto and P. scapulatus. The prevalence in P. poliocephalus varied across its distribution range with 15% in the central biogeographic areas (central Queensland and New South Wales) and 1% in the southern-most edge (South Australia) of its range. Sequencing of five genes revealed high genetic similarity in Hepatocystis of P. poliocephalus independent of sampling location. Phylogenetic analysis placed these parasites with Hepatocystis from other Pteropus species from Australia and Asia. While numerous haplotypes were identified among sequences from the Pteropus hosts, no patterns of host specificity were recovered within the Pteropus-specific parasite group.