The application of genome-wide cytonuclear molecular data to identify management and adaptive units at various spatio-temporal levels is particularly important for overharvested large predatory organisms, often characterized by smaller, localized populations. Despite being “near threatened”, current understanding of habitat use and population structure of Carcharhinus galapagensis is limited to speciﬁc areas within its distribution. We evaluated population structure and connectivity across the Paciﬁc Ocean using genome-wide single-nucleotide polymorphisms (~7200 SNPs) and mitochondrial control region sequences (945 bp) for 229 individuals. Neutral SNPs deﬁned at least two genetically discrete geographic groups: an East Tropical Paciﬁc (Mexico, east and west Galapagos Islands), and another central-west Paciﬁc(Lord Howe Island, Middleton Reef, Norfolk Island, Elizabeth Reef, Kermadec, Hawaii and Southern Africa). More ﬁne-grade population structure was suggested using outlier SNPs: west Paciﬁc, Hawaii, Mexico, and Galapagos. Consistently, mtDNA pairwise ΦST deﬁned three regional stocks: east, central and west Paciﬁc. Compared to neutral SNPs (FST=0.023–0.035), mtDNA exhibited more divergence (ΦST= 0.258–0.539) and high overall genetic diversity (h = 0.794 ±0.014; π = 0.004 ± 0.000), consistent with the longstanding eastern Paciﬁc barrier between the east and central–west Paciﬁc. Hawaiian and Southern African populations group within the west Paciﬁc cluster. Effective population sizes were moderate/high for east/west populations (738 and 3421, respectively). Insights into the biology, connectivity, genetic diversity, and population demographics informs for improved conservation of this species, by delineating three to four conservation units across their Paciﬁc distribution. Implementing such conservation management may be challenging, but is necessary to achieve long-term population resilience at basin and regional scales.