While the occurrence of separate sexes among individuals is commonplace in most animals, only around 10% of the flowering plants exhibit this condition (botanically termed “dioecy”). In the economically important Nightshade Family (Solanaceae), just 1% of the species exhibit a dioecious sexual system, with nearly all occurrences happening within the “spiny solanums” of the Australian Monsoon Tropics. In these species, males present morphologically as males; but, fascinatingly, plants that appear to be bisexual in form produce non-functional pollen that renders those individuals female in function. The origins of this condition in this Australian lineage and its relationship to other cosexual systems exhibited by closely-related species have been the subject of study for decades – work that as generated multiple new species descriptions plus inferences related to seed dispersal, pollination, and population genetics. Our current work aims to illuminate the evolutionary history of the lineage using targeted enrichment data, evaluate areas and potential sources of phylogenetic conflict, reconstruct the evolution of diverse breeding systems, and revisit previous hypotheses regarding reproductive characters. We provide a framework of evolutionary relationships in Australian spiny Solanum, with detected discordance among gene trees highlighting a complex history that includes rapid speciation, incomplete sorting of ancestral variation, and hybridization. Outcomes related to the evolution of diverse reproductive traits suggests that sexual system transitions in this group are not only more common than previously thought, but also underlie an ongoing radiation requiring further field-based and collections-based taxonomic effort.