Purpose <p><i>Oswaldofilaria bacillaris</i> is the type species of the genus, but its morphology remains little known and partially contradictory. Moreover, there are no genetic data and scanning electron microscopical observations on the species, like in most <i>Oswaldofilaria</i> spp. The phylogenetic relationships among <i>Oswaldofilaria</i> spp. are practically unknown. This study aimed to evaluate the detailed morphology of <i>O</i>. <i>bacillaris</i>, provide its first genetic characterization, and discuss the phylogenetic relationships within <i>Oswaldofilaria</i>.</p> Methods <p>Parasites infecting the body cavity of <i>Caiman yacare</i> in Pantanal wetlands, Mato Grosso do Sul, Brazil, were collected and processed for morphological studies using light and scanning electron microscopy. Genetic characterization was based on partial sequences of 18S and 28S rDNA. A phylogeny was reconstructed based on 28S sequences including all <i>Oswaldofilaria</i> available.</p> Results <p>Nematodes were assigned to <i>O</i>. <i>bacillaris</i> mainly based on the oral opening markedly displaced ventrally. Males had seven pairs of caudal papillae encircling the cloaca, and their two most posterior pairs were hardly visible, which is also characteristic in other congeners. Moreover, a delicate area rugosa previously unreported in the species was observed. <i>Oswaldofilaria bacillaris</i> formed a monophyletic assemblage with the congeners, being sister to <i>O</i>. <i>chabaudi</i>, and <i>O</i>. <i>petersi</i> was basal, these last two parasites of lizards.</p> Conclusion <p>The present findings strengthened the specific diagnosis of <i>O</i>. <i>bacillaris</i> and elucidated the morphological contradictions. The phylogeny reinforced the hypotheses that <i>Oswaldofilaria</i> emerged in lizards and colonized crocodilians by host switch, and reduction in number of caudal papillae in males is a derived feature.</p>