In Australia, climate change and continental drift have given rise to a complex biota comprising mesic specialists, arid-adapted lineages, and taxa that have arrived on the continent from Asia. We explore the phylogenetic diversity and biogeographic history of the Australian trapdoor spider genus Conothele Thorell, 1878 that is widespread in Australia’s monsoonal tropics and arid zone. We sequenced three mtDNA and five nuDNA markers from 224 specimens. We reconstructed the phylogenetic relationships among specimens and estimated the number of operational taxonomic units (OTUs) using species delimitation methods. The timing of divergences was estimated and ancestral area reconstructions were conducted. We recovered 61 OTUs, grouped into four major clades; a single clade represented by an arboreal ecomorph, and three fossorial clades. The Australian Conothele had a crown age of ~19 million years, and ancestral area reconstructions showed a complex history with multiple transitions among the monsoonal tropics, central arid zone, south-west and Pilbara bioregion. Conothele arrived on the continent during periods of biotic exchange with Asia. Since then, Conothele has colonised much of the Australian arid and monsoonal zones, during a period of climatic instability. The Pilbara bioregion harbours high lineage diversity, emphasising the role of climate refugia.