The genetic structure of parasite populations is affected by various factors such as host–parasite interactions, life‐history strategies, and the evolutionary histories of both interacting organisms. In this study, we investigated the distribution, prevalence, and population‐genetic structure of Icosiella neglecta (Spirurida, Onchocercidae), a nematode parasite found in Ranidae frogs. We reported this parasite from eight species of water frogs (genus Pelophylax) in Europe, the Middle East, and Central Asia. Its prevalence across investigated localities varied from 3.03% to 95.83%. Based on nucleotide variation in a 28S ribosomal RNA gene, all investigated I. neglecta sequences formed a well‐supported phylogenetic clade and were placed in the sister position to the genus Ochoterenella. Despite the substantial genetic variability in a mitochondrial cytochrome c oxidase subunit I (COI) fragment (33 unique haplotypes recognized among 91 sequences), we found only weak population‐genetic structure across the study area. There was no obvious association of COI haplotypes with geography, except haplotypes from eastern Turkey, Lebanon, and Iraq which formed a homogeneous, albeit only weakly differentiated group. The historical demographic analyses suggest that the species underwent a sudden and relatively recent population expansion. According to our results, we assume that the population‐genetic structure of I. neglecta might be linked to the evolutionary history and dispersal of its dipteran vectors than water frog hosts.