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The passerine family Meliphagidae (the honeyeaters) comprises 175-180 species in 40-50 genera. It is an iconic element of the Australo-Papuan avifauna and also occurs in Indonesia and on remote Pacific Ocean islands. Building on previous molecular studies that have pioneered a renewed understanding of the family’s circumscription and systematics, we present an updated phylogenetic and systematics synthesis of honeyeaters derived from 112 mostly Australian, New Guinean and Wallacean species- and subspecies-rank taxa aligned across 9246 positions spanning four mitochondrial and four nuclear genes. We affirm many of the recent changes advocated to the group’s genus-level systematics and offer some further refinements. The group’s radiation appears to coincide broadly with the aridification of Australia in the Miocene, consistent with the time of origin of diversification of extant lineages in several other groups of Australian organisms. Most importantly, the complexity of the biogeography underlying the group’s spectacular radiation, especially within Australia, is now apparent. Foremost among such examples is the robust evidence indicating that multiple, independent lineages of honeyeaters, including several monotypic genera, are endemic to the Australian arid zone, presumably having diverged and evolved within it. Also apparent and warranting further study are the phenotypic diversity among close relatives and the remarkably disjunct distributions within some clades, perhaps implying extinction of geographically intermediate lineages. Given such complexity, understanding the evolution of this radiation, which has thus far been intractable, relies on integration of molecular data with morphology, ecology and behaviour.