An important goal of comparative and functional genomics is to connect genetic polymorphisms to phenotypic variation. Leopards (Panthera pardus) from northern South Africa are particularly diverse, as here a unique colour morph occurs, as well as two deeply diverged southern (SA) and central African (CA) mitochondrial clades, stemming from Pleistocene refugia. Here, we present the first whole genomes of a red leopard and a black (captive) leopard, and wildtypes belonging to the CA and SA mitochondrial clades, to evaluate genome-wide diversity, divergence, and high impact mutations that may relate to their phenotype. In the black leopard, we found long runs of homozygosity (ROHs), low nucleotide diversity across the genome, and a large number of homozygous structural variants, likely resulting from inbreeding to maintain this colour morph in captivity. In red leopards, ROHs were slightly longer compared to wildtype leopards, with potential deleterious mutations relating to its phenotype, including impaired vision. When assessing population structure, we found no divergence between CA and SA leopards and the rest of Africa, whether comparing single nucleotide or structural variants. This illustrates the homogenizing effect of introgression, and highlights that although leopards in northern South Africa may be phenotypically unique, they are not genetically different.