Understanding plant local adaptation from a genomic perspective has become a key research area given recent climate challenge and the potential need for conservation of genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems and demographic histories. European aspen (Populus tremula) is a dioecious and obligately outbreeding tree species that grows across Eurasia but that also occurs in relatively isolated parts of the distribution range. Adaptation in European aspen shows evidence for clinal variation, likely due the response to selection along environmental gradients, in key phenology traits. There is also evidence for the occurrence of multiple hybrid zones among divergent post-glacial lineages that likely persist under migration-selection balance. We evaluated signatures of local adaptation across Europe by means of whole genome re-sequencing of a collection of 411 aspens spanning Eastern, Western and Northern Europe. Using different population genomic estimators, we dissected admixture patterns between aspen lineages and detected strong signals of adaptive introgression between Nordic populations in a genome region harbouring a large-effect locus that has contributed to adaptation to the short growing seasons characteristic of northern Scandinavia. Furthermore, we detected shared signals of balancing selection, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results highlight the complex adaptive history of aspens following the last glaciation in Northern Europe and emphasise the importance of migration-selection balance underlying the genetic architecture of key adaptive quantitative traits.