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Orthotyline plant bugs inhabiting the southern conifer genus Callitris in Australia are investigated and classified systemically for the first time, with the description of 5 new genera and 32 new species from Australia. The five new callitroid-inhabiting Orthotylini genera proposed are Avititerra, Blattakeraia, Callitricola, Erysivena, and Ngullamiris. The 32 new species accommodated by these genera are: Avititerra lepidothrix, A. xerophila, Blattakeraia actinostrobi, B. hochuli,Callitricola ballina, C. boorabbin, C. cordylina, C. finke, C.finlayae, C. gammonensis, C. graciliphila,C. parawirra, C. pullabooka, C. silveirae, C. tatarnici, C. wiradjuri, C. wollemi, Erysivena apta, E.bundjalung, E. drepanomorpha, E. emeraldensis, E. endlicheriphila, E. kalbarri, E. majori, E.mareeba, E. molloy, E. notodytika, E. paluma, E. schuhi, E. schwartzi, E. sydneyensis, and Ngullamiriswhadjuk. A key to the newly described Australian taxa, habitus photographs of all species, illustrations of male and female genitalia, and scanning electron micrographs of representative species are given. A phylogenetic analysis of these callitroid-inhabiting Orthotylini was undertaken, incorporating described Orthotylus Fieber species extralimital to Australia and other recently described Australian Orthotylini. Callitris host plants are mapped to the implied-weights phylogenetic analysis, and their associations are discussed. Associations between related species of Orthotylini and related species of Callitris were detected, as were three independent colonisations by a paraphyletic assemblage of callitroid-inhabiting Orthotylini. Generic concepts within Orthotylini are discussed, with reference to Orthotylus species extralimital to Australia and includes a comparison of key character systems. It is demonstrated that the endosomal spicule characters are primary determinants of generic limits in the Orthotylini, which are supported by other characters of the male and female genitalia and external characters.