Speciation is a continuous process and analysis of species pairs at, "different stages of divergence provides insight into how it unfolds. Spanning the speciation continuum stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However attention has largely focused on young postglacial species pairs with little known of the genomic signatures of divergence and introgression in older systems. The Japanese stickleback species pair Gasterosteus aculeatusG. nipponicus which co-occur in the Japanese islands is at a late stage of speciation. Here we use coalescent analyses and Approximate Bayesian computation to show that the two species split approximately 0.68-1 million years ago but that they have continued to hybridise at a low rate throughout divergence. Population genomic data revealed that high levels of genomic differentiation are maintained across the majority of the genome when gene flow occurs. However despite this we identified multiple small regions of introgression strongly correlated with recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow, composed of the Pacific Ocean three-spined stickleback and the Japan Sea stickleback.