Although local adaptation plays a fundamental role in maintaining adaptive genetic variation as a response to changing environments, its underlying genetic mechanisms remains poorly understood. In this study, we integrate “top-down” and “bottom-up” approaches to search for genomic signatures of local adaptation in Populus tremula along a latitudinal gradient across Sweden. We find that a majority of single nucleotide polymorphisms (SNPs) (~95%) identified as being involved in local adaptation are tightly clustered in a single genomic region on chromosome 10. This region harbors the candidate gene FLOWERING LOCUS T2 (FT2) that has long been known to play important roles in the regulation of growth cessation and dormancy induction in perennial plants. Our results provide empirical evidence suggesting that in the context of high rates of gene flow, the genomic architecture of local adaptation tends to enrich for few large-effect and/or tightly clustered loci rather than many independent loci of small effect. The signatures of selection at the candidate region are mostly consistent with soft selective sweeps, where different adaptive haplotypes originating from standing genetic variation sweep to high frequency in different latitudinal regions. In particular, we identify a recent and strong selective sweep that is regionally restricted to the northernmost populations. This indicates that high-latitude populations likely have undergone a stronger adaptive response to the greater environmental perturbation during the post-glacial colonization of northern Scandinavia.