Multilocus studies in phylogenetics and comparative phylogeography have the power to explore a broader spectrum of evolutionary questions than either discipline has alone. To examine the origins of sympatry in a group of closely related birds of mostly mesic eucalypt woodlands in Australia, we reconstructed the relationships among species of Entomyzon and Melithreptus honeyeaters (Aves: Passeriformes: Meliphagidae) using a mitochondrial marker, ND2, and six non-coding nuclear loci (total 4719 base pairs). By sampling across the geographical range of each species, we studied not only their phylogenetic relationships to each other but also the spatial distribution of their genetic diversity. We tested several biogeographic hypotheses concerning the role of Pleistocene environmental change in Australia. Phylogenetic gene trees support the current understanding of E. cyanotis as the sister to Melithreptus. Non-monophyly of M. lunatus in Australia's southern temperate woodlands highlights the need for a revision of systematics within Melithreptus. Phylogeographic analysis of the three northern species in Australia's monsoon tropics, M. gularis, M. albogularis and E. cyanotis, suggests that the roles of the Carpentarian and Torresian Barriers in shaping geographic structure in each of the species have been more complex and temporally dynamic than earlier morphology-based arguments of vicariance had suggested. We discuss their roles as ecological filters as well as barriers.