The brittle star Ophiothrix suensonii is a common coral reef sponge commensal with high dispersal potential. Here, we utilize COI sequence data from 264 O. suensonii individuals collected from 10 locations throughout Florida and the Caribbean to investigate dispersal dynamics and demographic history. Locations separated by up to 1,700 km lacked genetic differentiation, confirming the ability for long-range dispersal. However, significant differentiation was detected among other regions. Samples from Utila, Honduras showed the greatest differentiation, suggesting that the circulation of the Mesoamerican gyre could be a significant factor restricting gene flow in this region. Demographic analyses provided strong evidence for a population expansion, possibly out of Florida, through the Caribbean, and into Honduras, which commenced in the early Pleistocene. However, the presence of a clade of rare haplotypes, which split much earlier (mid-Pliocene), indicates that O. suensonii persisted long before its recent expansion, suggesting a cyclic history of population contraction and expansion. Finally, patterns of gene flow are not concordant with contemporary surface currents; rather, they reflect historical movements possibly linked with changes in circulation during periods of Pleistocene climate change.