Understanding the origin of species is one of the major pursuits in evolutionary biology. As populations undergo the speciation process, their genomic divergence is influenced by selection, gene flow, and genetic drift. These forces act and interact in a context of varying geographic and genomic landscapes. Furthermore, the importance of these forces may change throughout the speciation continuum, from early population divergence to reproductive isolation. To understand how genome divergence accumulates during the speciation process, we took a comparative approach using population pairs at different stages of the speciation process. Using multiple species within the bird superfamily comprising the honeyeaters, fairywrens, gerygones, and allies, we developed a new comparative system to study speciation, showed how the extent of gene flow changes through the speciation process given different geographic connectivity, and showed how this change in divergence varies across the genome through speciation.