Invasive non-native species are recognized as a serious threat to the native biodiversity of the areas they colonize. The subterranean spider Howaia mogera (Yaginuma 1972) (syn. Nesticella mogera) is considered a highly invasive non-native species rapidly expanding its geographical range from Asia across the European continent and to remote oceanic islands. Due to its preference for moist, dark, and climatically stable habitats, including caves, this spider represents a potential threat to the endemic fauna living in the forest litter and subterranean environments. Nevertheless, the origin, biogeography, patterns of colonization, and niche preference of H. mogera remain unexplored. In this study, we reconstructed the phylogeography of the species combining a multi-locus phylogenetic analysis and a niche modeling approach. Our results confirm the center of origin of H. mogera in southern China, from where the species naturally spread and diversified in eastern Asia during the Pleistocene Epoch. Its expansion into non-native areas occurred only recently, possibly as a consequence of human-mediated passive transportation and in conjunction with a shift in the habitat preference of the species. Non-native populations have shifted from an original preference for a subterranean lifestyle to more generalist conditions. This change has allowed them to exploit a wider breadth of habitats and has facilitated their expansion in Europe and remote oceanic islands. Yet, the retention of the original subterranean habitat preferences in these non-native populations poses a conservation threat to specialized and fragile subterranean ecosystems, which H. mogera can efficiently exploit in invaded areas. Our study underscores the importance of comprehending phylogeography and niche dynamics in invasive non-native species to predict and manage their future expansions. We further highlight the urgency of monitoring H. mogera's spread worldwide, particularly in Southern Europe, to protect fragile invaded ecosystems.