Understanding the factors that determine the realized and potential distribution of a species requires knowledge of abiotic, physiological, limitations as well as ecological interactions. Entomopathogenic fungi of the order Laboulbeniales specialize on arthropod hosts and are typically thought to be highly specialized on a single host or closely related group of hosts. Because infections are solely transmitted through direct contact of the hosts, the host ecology to a large extent determines the distribution and occurrence of the fungus. We examined ~20,000 fruit flies (Diptera: Dacinae) collected in Malaysia, Sulawesi, Australia and the Solomon Islands between 2017–2019 for ectoparasitic fungal infections and found 197 infected flies across eight different Bactrocera species. Morphology and small subunit (18S) DNA sequences both support that the infections are from a single polyphagous fungal species. This presents the paradox of why S. dacinus is not more common when its hosts are widespread and ubiquitous. In addition, the hosts are all Bactrocera, a genus with ~480 species, but many sympatric Bactrocera were never infected. Host-selection does not appear to be phylogenetically correlated. Our results show that a single fungus species can be found on different host species in different continents. We discuss factors that might be involved in determining the host and distribution range of S. dacinus, such as host resistance, and discuss the potential for population control of agriculturally important hosts, such as the pestiferous Oriental fruit fly Bactrocera dorsalis and the Queensland fruit fly B. tryoni.