In tropical rainforests, insects show especially high species richness and local endemism of species relative to vertebrates. One possible cause is that insects respond to historical fluctuations of rainforests on a smaller spatial scale than do vertebrates. To evaluate this hypothesis, we combine environmental niche models and mitochondrial DNA phylogeography for two pairs of sister species of the dung beetle genus Temnoplectron (T. aeneopiceum–T. subvolitans and T. politulum–T. reyi) from the rainforests of northeastern Australia, where climate-driven rainforest fluctuations in the Quaternary have strongly influenced genetic and species diversity of vertebrates. Within both species pairs, the bioclimatic niche was conserved, but the T. aeneopiceum–T. subvolitans species pair had the narrower environmental range, and thus more restricted potential distribution. Coalescent analyses indicated Late Pliocene or Early Pleistocene divergences for both species pairs, and earlier speciation in (T. aeneopiceum–T. subvolitans) than in (T. politulum–T. reyi). Phylogeographic structure in (T. aeneopiceum–T. subvolitans) was more pronounced than in (T. politulum–T. reyi), with significant isolation-by-distance in the former species-pair only. Nested clade and coalescence analyses indicated local range expansions for the T. aeneopiceum–subvolitans species pair and range-wide expansion for both T. politulum and T. reyi. We suggest that stronger phylogeographic structure and earlier divergence in (T. aeneopiceum–T. subvolitans) than in (T. politulum–T. reyi) reflects a stronger influence of environmental barriers to gene flow under the present climate and greater sensitivity to warmer and drier periods of the Quaternary. The two species pairs evidently responded to Quaternary rainforest fluctuations at spatial scales similar to those seen within low-vagility species of vertebrate. Despite this similarity of scale, these insect lineages are reproductively isolated at parapatric boundaries, whereas analogous lineages of vertebrates often are not. We suggest that rapid evolution of genitalia may facilitate geographic speciation in rainforest beetles.