The metagenomics revolution has started to unravel the mysteries of microbial communities (comprising viruses, bacteria and eukaryotic microbes) within northern hemisphere ticks where arthropod co-infections and co-transmission of pathogens to vertebrate hosts are well known. Increasingly the role of endosymbionts as modulators of that transmission, and as potential pathogens in their own right is being recognised. What is the situation in Australia where concern about tick-borne illness in humans gathers apace, and microbiome research offers the potential to inform this contentious debate? Despite sharing some taxa with Ixodidae of other continents, approximately 65 endemic tick species are confined to the Australian continent, its offshore islands and New Guinea, and have evolved with the unique mammalian and monotremal fauna for millennia. Studies of Australian indigenous ticks, collected nationwide from the environment and a wide range of vertebrate hosts (including humans), and tested by high-throughput next generation sequencing technology, are starting to reveal rich and diverse microbiomes. Endosymbionts (e.g. Candidatus Midichloria mitochondrii, Coxiella, Francisella and Rickettsia spp.) are prevalent in ticks. These and the genera of familiar pathogens (e.g. Anaplasma, Babesia, Borrelia, Ehrlichia, and Neoehrlichia spp.) have now been identified locally, yet are distinct from their northern hemisphere relatives. We stand on the threshold of gaining a deeper understanding of the microbes of Australian ticks, which might provide answers to important questions about their disease-causing potential.