This work presents the first hypothesis of phylogenetic relationships among all 40 genera of the treehopper tribe Terentiini (Hemiptera : Membracidae : Centrotinae). This phylogeny, based on a parsimony analysis of 77 morphological characters, made possible an analytical approach to determining the likely ancestral host-plant family and geographic distribution of the tribe, based on present-day hosts and distributions. Of Australia’s 37 treehopper genera, 36 belong to the tribe Terentiini, with their centre of diversity in Queensland (30 genera). Optimisations of present-day distributions mapped on our phylogeny suggest that the ancestor of the tribe occurred in the Australian region, around north-eastern Australia (Queensland) and New Guinea (which has 8–10 terentiine genera). Subsequent dispersals from the Australian region (with 37 genera) took the tribe to the Indomalayan (11 genera) and Palaearctic (1 genus) regions. At least 13 terentiine genera include representatives that occur beyond the borders of Australia and New Guinea. Notable among the migrant lineages is the clade ‘Polonius + (Bulbauchenia + (Funkhouserella + Pyrgonota))’, which includes genera with such extraordinary pronotal modifications that some members were previously placed in separate tribes (Bulbaucheniini or Funkhouserellini). Members of this remarkable breakaway clade are known from Australia (Polonius only), Indonesia, the Malay Peninsula, Thailand, the Philippines, southern China (Taiwan and Hainan Island) and Japan. With regard to terentiine host plants, optimisations of present-day host associations point to the Leguminosae as the ancestral host family, even though plant families of Gondwanan origin, especially Myrtaceae and Proteaceae, are also prominent terentiine hosts. The overall evidence to date indicates that Terentiini are not a remnant of the early Gondwanan fauna, but rather a more recent tribe derived from Indomalayan ancestors.