Seagrasses are globally declining due to direct human impacts and climate change. Effective measures of seagrass conservation, management, and restoration require an understanding of the variation in reproductive strategies. Here, we examine how reproductive strategies differ between core and range-edge populations for the widely distributed but regionally threatened seagrass species Enhalus acoroides, spanning more than 5000 km. We fill an important gap in geographic coverage by including western Pacific islands, a region often overlooked in Indo-Pacific seagrass genetic studies. Specifically, we assess genotypic diversity, clonal structure, and genetic connectivity for thirty-six populations across islands or small island groups throughout Southeast Asia and Micronesia. Near the range edge, exceptionally low genotypic richness was found for geographically isolated islands in Micronesia (Guam and Saipan), with a millennia-old clone being prevalent across all meadows and shared between islands at more than 200 km distance, a phenomenon not previously documented for Indo-Pacific seagrass species. In contrast, core populations around small islands in Southeast Asia, that are in close vicinity to the mainland or large islands, exhibited high genotypic diversity and small clonal sizes. We propose that limited long-distance dispersal of propagules to isolated islands near the species’ range edge drives reduced levels of sexual reproduction and facilitates extreme clonality in E. acoroides. The strong variation in genotypic diversity and clonal structure between core and range-edge populations suggest regional differences in the resilience of E. acoroides meadows, highlighting the need for targeted conservation measures and restoration efforts.