The oceanic whitetip shark, Carcharhinus longimanus, is a circumtropical pelagic shark of high conservation concern (IUCN Red List: “Critically Endangered” in the Western North and Western Central Atlantic and “Vulnerable” globally). I present the first, population genetic assessment of the oceanic whitetip shark on a global scale, based on analysis of two mitochondrial genome regions (entire 1066-1067 bp control region and 784 bp partial ND4 gene), and nine nuclear microsatellite loci. No population structure was detected within the Western Atlantic. However, highly significant population structure was detected between Western Atlantic and Indo-Pacific Ocean sharks across all markers. Additionally, a nominally significant signal of matrilineal structure between the Indian and Pacific Ocean sharks was detected by AMOVA and pairwise tests of the ND4 gene only (pairwise ΦST = 0.051, P = 0.046; pairwise Jost’s D = 0.311, 95% CI = 0.020, 0.0614). Although significant inter-basin population structure was evident, it was associated with deep phylogeographic mixing of mitochondrial haplotypes and evidence of contemporary migration between the Western Atlantic and Indo-Pacific Oceans. I theorize that semi-permeable thermal barriers are responsible for the differentiation between the Western Atlantic and Indo-Pacific set in a framework of global phylogeographic mixing. Relatively low mtDNA genetic diversity (concatenated mtCR-ND4 nucleotide diversity π = 0.32% ± 0.17%) compared to other circumtropical elasmobranch species raises potential concern for the future genetic health of this species. Overall, significant population structure exists, at a minimum, between the Western Atlantic and Indo-Pacific Ocean, and effective management strategies must take this into consideration.