Large pelagic vertebrates pose special conservation challenges because their movements generally exceed the boundaries of any single jurisdiction. To assess the population structure of whale sharks (Rhincodon typus), we sequenced complete mitochondrial DNA control regions from individuals collected across a global distribution. We observed 51 single site polymorphisms and 8 regions with indels comprising 44 haplotypes in 70 individuals, with high haplotype (h = 0.974 ± 0.008) and nucleotide diversity (π = 0.011 ± 0.006). The control region has the largest length variation yet reported for an elasmobranch (1143–1332 bp). Phylogenetic analyses reveal no geographical clustering of lineages and the most common haplotype was distributed globally. The absence of population structure across the Indian and Pacific basins indicates that oceanic expanses and land barriers in Southeast Asia are not impediments to whale shark dispersal. We did, however, find significant haplotype frequency differences (amova, FST = 0.107, P < 0.001) principally between the Atlantic and Indo-Pacific populations. In contrast to other recent surveys of globally distributed sharks, we find much less population subdivision and no evidence for cryptic evolutionary partitions. Discovery of the mating and pupping areas of whale sharks is key to further population genetic studies. The global pattern of shared haplotypes in whale sharks provides a compelling argument for development of broad international approaches for management and conservation of Earth's largest fish.