Widespread tree species span large climatic gradients that often lead to high levels of local adaptation and phenotypic divergence across their range. To evaluate the relative roles of selection and drift in driving divergence in phenotypic traits, we compared molecular and quantitative genetic variation in Populus fremontii (Fremont cottonwood), using data from > 9000 SNPs and genotypes from 16 populations reciprocally planted in three common gardens that span the species’ climatic range. We present three major findings: 1) There is significant within- and among-population variation in functional traits expressed in each of the common gardens. 2) There is evidence from all three gardens that population divergence in leaf phenology and specific leaf area has been driven by divergent selection (QST > FST). In contrast, QST-FST comparisons for performance traits like height and basal diameter were highly dependent on growing environment, indicating divergent, stabilizing, or no selection across the three gardens. We show this is likely due to local adaptation of source populations to contrasting growing environments. 3) Climate is a primary selective force driving trait divergence, where the traits showing the strongest correlations with a genotype’s provenance climate also had the highest QST values. We conclude that climatic gradients have contributed to significant phenotypic differences and local adaptation in Fremont cottonwood. These results are important because as climate is changing much more rapidly, traits such as phenology that are finely tuned to local conditions may now be subject to intense selection or quickly become maladaptive.