Abstract Geographically connected species pairs with weakly differentiated genomes could either represent cases of genomic homogenization in progress or of incipient parapatric speciation. Discriminating between these processes is difficult because intermediate stages of either may produce weakly differentiated genomes that diverge at few locations. We used coalescent modelling applied to a genome‐wide sample of SNPs to discriminate between speciation with gene flow and genomic homogenization in two phenotypically distinct but genomically weakly diverged species of elevationally replacing Ramphocelus tanagers, forming a hybrid zone in the Andean foothills. We found overwhelming support for a model of genomic homogenization following secondary contact. Simulating under this model suggested that our species pair was differentiated ( F ST = 0.30) at secondary contact but that most of the genome has rapidly homogenized during 254 Ky of high gene flow towards the present ( F ST = 0.02). Despite extensive genome‐wide homogenization, plumage remains distinctive with a narrower than expected geographic cline width, indicating divergent selection on colour. We found two SNPs significantly associated with plumage colour, which retain moderately high F ST . We conclude that the majority of the genome has fused, but that divergent selection on select loci probably maintains the geographically structured colour differences between these incipient species.