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Why do some genera radiate, whereas others do not? The genetic structure of present-day populations can provide clues for developing hypotheses. In New Zealand, three Cicadidae genera are depauperate [Amphipsalta (three species), Notopsalta (one species) and Rhodopsalta (three species)], whereas two have speciated extensively [Kikihia (~30 species/subspecies) and Maoricicada (~20 species/subspecies). Here, we examine the evolution of Rhodopsalta, the last New Zealand genus to be studied phylogenetically and phylogeographically. We use Bayesian and maximum-likelihood analyses of mitochondrial cox1 and nuclear EF1α gene sequences. Concatenated and single-gene phylogenies for 70 specimens (58 localities) support its monophyly and three described species: Rhodopsalta cruentata, Rhodopsalta leptomera and Rhodopsalta microdora, the last taxon previously regarded as uncertain. We provide distribution maps, biological notes and the first descriptions of diagnostic songs. We show that both R. cruentata and R. microdora exhibit northern and southern genetic subclades. Subclades of the dry-adapted R. microdora clade show geographical structure, whereas those of the mesic R. cruentata and sand-dune specialist R. leptomera have few discernible patterns. Genetic, bioacoustical and detailed distributional evidence for R. microdora add to the known biodiversity of New Zealand. We designate a lectotype for Tettigonia cruentataFabricius, 1775, the type species of Rhodopsalta.