Host-associated adaptation is emerging as a potential driver of population differentiation and speciation for marine organisms with major implications for ecosystem structure and function. Coralliophila abbreviata are corallivorous gastropods that live and feed on most of the reef-building corals in the tropical western Atlantic and Caribbean. Populations of C. abbreviata associated with the threatened acroporid corals, Acropora palmata and A. cervicornis, display different behavioral, morphological, demographic, and life-history characteristics than those that inhabit other coral host taxa, indicating that host-specific selective forces may be acting on C. abbreviata. Here, we used newly developed polymorphic microsatellite loci and mitochondrial cytochrome b sequence data to assess the population genetic structure, connectivity, and demographic history of C. abbreviata populations from three coral host taxa (A. palmata, Montastraea spp., Mycetophyllia spp.) and six geographic locations across the Caribbean. Analysis of molecular variance provided some evidence of weak and possibly geographically variable host-associated differentiation but no evidence of differentiation among sampling locations or major oceanographic regions, suggesting high gene flow across the Caribbean. Phylogenetic network and bayesian clustering analyses supported a hypothesis of a single panmictic population as individuals failed to cluster by host or sampling location. Demographic analyses consistently supported a scenario of population expansion during the Pleistocene, a time of major carbonate reef development in the region. Although further study is needed to fully elucidate the interactive effects of host-associated selection and high gene flow in this system, our results have implications for local and regional community interactions and impact of predation on declining coral populations.