Studying wildlife taxonomic diversity and identifying distinct populations has traditionally been largely based on morphology and geographic origin. More recently, this method has been supplemented by genetic data from the mitochondrial genome. However, this is limited as only maternally inherited and may not reflect the true nature of a population’s genetics. Within the giraffe (Giraffa spp.), subspecies and unique populations were successfully characterized using both mitochondrial and genomic DNA studies, which led to new insights and, in some cases, unexpected results that required further verification. Here, we sequenced the genomes of 85 southern giraffe (G. giraffa) individuals from ten populations across southern Africa for a detailed investigation into the genetic diversity and history of its two subspecies, the Angolan (G. g. angolensis) and the South African (G. g. giraffa) giraffe. While the overall genotypes show low levels of runs of homozygosity compared to other mammals, the degree of heterozygosity is limited despite the large population size of South African giraffe. The nuclear genotype is largely congruent with the mitochondrial genotype. However, we have identified that the distribution of the Angolan giraffe is not as far east as indicated in an earlier mitochondrial DNA study. Botswana’s Central Kalahari Game Reserve giraffe are unique, with a clear admixture of Angolan and South African giraffe populations. However, the enigmatic desert-dwelling giraffe of northwest Namibia is locally distinct from other Angolan giraffe yet exhibits intra-subspecies signs of admixture resulting from a recent introduction of individuals from Namibia’s Etosha National Park. Whole genome sequencing is an invaluable and nearly indispensable tool for wildlife management to uncover genetic diversity that is undetectable through mitogenomic, geographical, and morphological means.