Adaptive differentiation in functional traits and their underlying loci can occur across a small geographic area if natural selection is stronger than the countervailing effects of gene flow and drift. We investigated this hypothesis in a long-lived, wind-pollinated species, Quercus rubra, across a fine spatial scale with a steep climate gradient. We examined phenotypic differentiation in a common garden study with eight populations sampled 0-160 km from the coast of Lake Superior. We estimated genomic differentiation for these and 22 additional populations from the same region, along with two populations of a congener, Quercus ellipsoidalis, using RAD-seq. We found a strong signal of population differentiation associated with climate in the common garden study, and differentiation was significantly associated with at least one climate factor for nine of ten measured traits. At the genomic level, we discovered widespread introgression from Q. ellipsoidalis into Q. rubra that increased with distance from the lake. Pairwise F_ST among Q. rubra populations was low, but both distance-based and environmental association analyses identified loci under selection, with one locus in common across all analyses (CalS10/GSL8). This locus was associated with the precipitation of the driest month, a climate factor that was also significant in the common garden analyses. In sum, this study reveals signatures of selection at the phenotypic and genomic level consistent with climate adaptation, a pattern that is usually seen across a much broader geographic scale.