Phylogenetic relationships within the genus Wyeomyia Theobald are presented, based on a cladistic analysis of 88 morphological characters (from adults, larvae, and pupae) of 38 named species and 1 unnamed species and 46 allozyme markers from a subset of 19 of these species. Two taxa are used as outgroup (Sabethes aurescens Lutz and Limatus durhami Theobald). The analysis indicates that, as currently defined, the genus Wyeomyia is not a monophyletic lineage: firstly, the genus Onirion Peyton and Harbach is nested within the genus Wyeomyia, and secondly, the subgenus Phoniomyia Theobald is a monophyletic lineage outside the genus Wyeomyia. Our results also demonstrate that the subgenera Cruzmyia Lane and Cerqueira, Decamyia Dyar, Dendromyia Theobald, Spilonympha Motta and Lourenço-de-Oliveira, and Prosopolepis Lutz are monophyletic lineages nested within the genus Wyeomyia. Triamyia Dyar is resurrected as a subgenus of Wyeomyia to include W. aporonoma Dyar and Knab and W. staminifera Lourenço-de-Oliveira, Motta, and Castro. The subgenus Miamyia Dyar is resurrected to include seven species: W. codiocampa Dyar and Knab, W. lutzi (Costa Lima), W. limai Lane and Cerqueira, W. serrata (Lutz), W. hosautos Dyar and Knab, W. oblita (Lutz), and W. sabethea Lane and Cerqueira.