The first occurrence of the cyanobacteriosponge Terpios hoshinota was reported from coral reefs in Guam in 1973, but was only formally described in 1993. Since then, the invasive behavior of this encrusting, coral-killing sponge has been observed in many coral reefs in the West Pacific. From 2015, its occurrence has expanded westward to the Indian Ocean. Although many studies have investigated the morphology, ecology, and symbiotic cyanobacteria of this sponge, little is known of its population genetics and demography. In this study, a mitochondrial cytochrome oxidase I (COI) fragment and nuclear ribosomal internal transcribed spacer 2 (ITS2) were sequenced to reveal the genetic variation of T. hoshinota collected from 11 marine ecoregions throughout the Indo-West Pacific. Both of the statistical parsimony networks based on the COI and nuclear ITS2 were dominated by a common haplotype. Pairwise F ST and Isolation-by-distance by Mantel test of ITS2 showed moderate gene flow existed among most populations in the marine ecoregions of West Pacific, Coral Triangle, and Eastern Indian Ocean, but with a restricted gene flow between these regions and Maldives in the Central Indian Ocean. Demographic analyses of most T. hoshinota populations were consistent with the mutation-drift equilibrium, except for the Sulawesi Sea and Maldives, which showed bottlenecks following recent expansion. Our results suggest that while long-range dispersal might explain the capability of T. hoshinota to spread in the IWP, stable population demography might account for the long-term persistence of T. hoshinota outbreaks on local reefs.