Sea cucumber populations are declining worldwide through overfishing. This is also the case for the greenfish Stichopus chloronotus in spite of its moderate commercial value. We studied asexual propagation of this fissiparous species at different geographic scales as well as the genetic population structure within and among two marine provinces: the Western Indian Ocean and the Tropical Southwestern Pacific. A total of 18 populations (n = 809 individuals) were sampled in both provinces encompassing three ecoregions (New Caledonia, western and northern Madagascar, Mascarene Islands) and genotyped using nine microsatellite loci, allowing the identification of repeated multi-locus genotypes. Populations presented low clonal richness with few clones and a high number of individuals per clone. No clones were shared among different islands. Within islands, members of the same clone could be found 3–15 km apart, indicating that asexual reproduction allows population maintenance at reef scales. Assignment tests and individual-based networks identified two isolated New Caledonian populations, while a third population was less differentiated to those from the Western Indian Ocean than to the two former. Regional ocean currents could explain these patterns. Within the Western Indian Ocean, differentiation indices were always high, indicating restricted gene flow among populations. Possible overfishing of S. chloronotus stock is evidenced by very low sample sizes (and in some cases, the absence) in spite of high sampling efforts [all around New Caledonia, Chesterfield/Bampton/Bellona Plateau (Coral Sea), north-east of Madagascar, Scattered Islands (Mozambique Channel)].