The incidence of introgression during the diversification process and the timespan following divergence when introgression is possible are poorly understood in the neotropics where high species richness could provide extensive opportunities for genetic exchange. We used thousands of genome‐wide SNPs to infer phylogenetic relationships, calculate ages of splitting, and to estimate the timing of introgression in a widespread avian neotropical genus of woodcreepers. Five distinct introgression events were reconstructed involving taxa classified both as subspecies and species including lineages descending from the basal–most split, dated to 7.3 million years ago. Introgression occurred between just a few hundred thousand to about 2.5 million years following divergence, suggesting substantial portions of the genome are capable of introgressing across taxa boundaries during a protracted time window of a few million years following divergence. Despite this protracted time window, we found that the proportion of the genome introgressing (6–11%) declines with the time of introgression following divergence, suggesting that the genome becomes progressively more immune to introgression as reproductive isolation increases.