The speed and magnitude of global change will have major impacts on riparian ecosystems, thereby leading to greater forest vulnerability. Assessing species’ adaptive capacities to provide relevant information for vulnerability assessments remains challenging, especially for nonmodel species like the North American Populus deltoides W. Bartram ex Marshall. The objective of this study was to understand how genomic diversity of this foundation species was shaped by its environment (climate, soil, and biotic interactions) to gauge its adaptive capacity. We used two complementary approaches to get a full portrait of P. deltoides genetic diversity at both the species and whole-genome ranges. First, we used a set of 93 nuclear and three chloroplastic SNP markers in 946 individuals covering most of the species' natural distribution. Then, to measure the degree of intraspecific divergence at the whole-genome level and to support the outlier and genomic-environment association analyses, we used a sequence capture approach on DNA pools. Three distinct lineages for P. deltoides were detected, and their current distribution was associated with abiotic and biotic variations. The comparison between both cpDNA and ncDNA patterns showed that gene flow between the lineages is unbalanced. The southern and northeastern populations may benefit from the input, through river flow, of novel alleles located upstream to their local gene pools. These alleles could migrate from populations that are already adapted to conditions that fit the predicted climates in the receiving local populations, hotter at the northeastern limit and drier in the Central United States. These “preadapted” incoming alleles may help to cope with maladaptation in populations facing changing conditions.