Adaptation of the annual cycles of growth initiation and cessation to the environment is critical for survival of woody plants. Thus, understanding the regulation of the seasonal cycles on perennial species is crucial for our ability to confidently predict how trees respond to local climate. This research will extend our knowledge on phenological responses of black poplar (Populus nigra), a European native species with substantial economic impact in worldwide active breeding programs. For this purpose, bud flush (BF) and bud set (BS) were taken as the cornerstones of the seasonal growth cycle in an integrative approach by dissecting the phenotypic level into several components. The genetic variability and the phenotypic plasticity of BF and BS were assessed in 13 natural metapopulations spanning 12° of latitude and grown in two common garden experiments in France and Italy. Genetic differences in the rates and degrees of adaptive responses to phenology between northern and southern populations were detected within and between sites. We found that broad-sense heritability for BF was generally higher (0.81 ≤ H2 ≤ 0.85) than for BS (0.35 ≤ H2 ≤ 0.54), suggesting that abundant genetic variation exists for phenological response to changes in the length of the growing season. QST values, which estimate the proportion of the total trait variation among populations were generally higher for BS (0.35 ≤ QST ≤ 0.47) than for BF (0.26 ≤ QST ≤ 0.33). As indicated by the considerable role of G×E interaction in the observed phenotypic variance, the studied metapopulations respond differently to the two sites. Furthermore, G×E interaction for BS was explained by rank and scale changes between locations, while it was mainly attributed to the differences in the scale of genotypic responses across sites for BF. These results provide new insights into the study of phenology in P. nigra germplasm and will speed up breeding to improve growth and adaptation to future climatic conditions