Even within an insect family famous for its morphological diversity, the treehopper subfamily Heteronotinae is a microcosm of pronotal variation, displaying remarkably dissimilar thoracic ornamentations among its ten included genera. Presented here is a reconstruction of heteronotine relationships based on DNA nucleotide sequence data from five nuclear and two mitochondrial genes from a comprehensive sample of ingroup taxa (including exemplars of all genera except for the monotypic Dysyncritus Fowler, 1895). Concordant phylogenetic estimates support the monophyly of Heteronotinae sensu stricto (i.e. excluding Darnoides Fairmaire, 1846), as well as the monophyly of the included genera Heteronotus Laporte, 1832, Nassunia Stål, 1862, Omolon Walker, 1862, Rhexia Stål, 1867, and Smiliorachis Fairmaire, 1846. Conversely, Anchistrotus Buckton, 1902, Allodrilus Evangelista, 2014 and Iria Stål, 1867 were not recovered as monophyletic, although topology comparison tests failed to reject the nonmonophyly of the latter two genera, nor Heteronotinae, as currently circumscribed. These results are interpreted in the context of available morphological evidence, which generally supports these findings. Also addressed here is the evolution of selected pronotal features representing major aspects of heteronotine morphology. Bayesian stochastic mapping of pronotal traits estimated multiple character state transitions, suggesting repeated acquisition of pronotal features, most of which have evolved independently within the diverse genus Heteronotus. These convergences may provide insight into the role of the pronotum in heteronotine groups that appear to serve different adaptive strategies, such as mimicry, crypsis and defence against predators. Furthermore, our results show a substantial diversity in need of formal description, including possible new genera, and several unique sexually dimorphic syndromes that may constitute a species complex within Heteronotus delineatus Walker, 1858. Nomenclatural changes are proposed for Nassunia nigromacula (Funkhouser, 1940) new combination and Smiliorachis inornata Stål, 1862 combination reinstated, which were found to be misplaced at the generic and subfamily levels according to our analyses.