Molecular phylogenetic analyses of 113 taxa representing Ascaridida, Rhigonematida, Spirurida and Oxyurida were used to infer a more comprehensive phylogenetic hypothesis for representatives of ‘clade III’. The posterior probability of multiple alignment sites was used to exclude or weight characters, yielding datasets that were analysed using maximum parsimony, likelihood, and Bayesian inference methods. Phylogenetic results were robust to differences among inference methods for most high-level taxonomic groups, but some clades were sensitive to treatments of characters reflecting differences in alignment ambiguity. Taxa representing Camallanoidea, Oxyurida, Physalopteroidea, Raphidascarididae, and Skrjabillanidae were monophyletic in all 9 analyses whereas Ascaridida, Ascarididae, Anisakidae, Cosmocercoidea, Habronematoidea, Heterocheilidae, Philometridae, Rhigonematida and Thelazioidea were never monophyletic. Some clades recovered in all trees such as Dracunculoidea and Spirurina included the vast majority of their sampled species, but were non-monophyletic due to the consistent behaviour of one or few ‘rogue’ taxa. Similarly, 102 of 103 clade III taxa were strongly supported as monophyletic, yet clade III was paraphyletic due to the grouping of Truttaedacnitis truttae with the outgroups. Mapping of host ‘habitat’ revealed that tissue-dwelling localization of nematode adults has evolved independently at least 3 times, and relationships among Spirurina and Camallanina often reflected tissue predilection rather than taxonomy.