Spotted owls (SO, Strix occidentalis) are a flagship species inhabiting old-growth forests in Western North America. In recent decades, their populations have declined due to ongoing reductions in suitable habitat caused by logging, wildfires, and competition with the congeneric barred owl (BO, Strix varia). The northern spotted owl (S. o. caurina) has been listed as “threatened” under the Endangered Species Act since 1990. Here we use an updated SO genome assembly along with 51 high-coverage whole-genome sequences to examine population structure, hybridization and recent changes in population size in SO and BO. We found that potential hybrids identified from intermediate plumage morphology were a mixture of pure BO, F1 hybrids and F1 x BO backcrosses. Also, while SO underwent a population bottleneck around the time of the Pleistocene – Holocene transition, their population sizes rebounded and show no evidence of any historical (i.e., 100 – 10,000 years ago) population decline. This suggests that the current decrease in SO abundance is due to events in the past century. Finally, we estimate that western and eastern BO have been genetically separated for thousands of years, instead of the previously assumed recent (i.e., <150 years) divergence. While this result is surprising, it is unclear where the ancestors of western BO lived after the separation. In particular, while BO may have colonized western North America much earlier than the first recorded observations, it is also possible that the estimated divergence time reflects unsampled BO population structure within central or eastern North America.