Introgression can introduce novel genetic variation at a faster rate than mutation alone, and result in adaptive introgression when adaptive alleles are maintained in the recipient genome over time by natural selection. A previous study from our group demonstrated adaptive introgression from Populus balsamifera into P. trichocarpa in a target genomic region. Here we expanded our local ancestry analysis to the whole genome of both parents to provide a comprehensive, unbiased view of introgression patterns and to identify additional candidate regions for adaptive introgression genome-wide. Populus trichocarpa is a large, fast-growing tree of mild coastal regions of the Pacific northwest, whereas P. balsamifera is a smaller stature tree of continental and boreal regions with intense winter-cold. The species are parapatric with extensive hybridization. Here, using local ancestry analysis, we detected asymmetric patterns of introgression across the whole genome of these two species of poplar trees adapted to contrasting environments, with stronger introgression from P. balsamifera to P. trichocarpa than vice versa. Admixed P. trichocarpa individuals showed more genomic regions with unusually high levels of introgression (19 regions) compared with admixed P. balsamifera (9 regions) but also the largest introgressed peak (1.02 Mb). Our analysis also revealed numerous candidate regions for adaptive introgression with strong signals of selection, notably related to disease resistance, and enriched for genes that may play crucial roles for survival and adaptation. Furthermore, we revealed overrepresentation of subtelomeric regions in P. balsamifera introgression into P. trichocarpa and possible protection of the sex-determining regions from interspecific gene flow.