In aspen and other plant species the effects of environment on phenotype are generally better characterized than genotypic influences. Furthermore, little is known about how genetic influences on tree phenotype change over time. We assessed clonal differences in 417 ramets, representing 18 clones, in a common garden of quaking aspen (Populus tremuloides Michx.) that have developed over 27 years. Genetic contributions to variation in physiology, growth, and vigor were determined over seasonal and multidecadal time scales. The 18 aspen clones exhibited wide-ranging phenotypic variation with two- to threefold differences in physiology and growth traits and more than sevenfold differences in canopy decline and mortality. For growth traits, strong genetic correlations (typically greater than 0.70) and heritability (estimates maintained in a range of 0.25 to 0.36), indicate that genotype had a moderate and consistent influence on growth over the three decades of the study. Physiological traits had much lower genetic correlations and heritability estimates, and they changed significantly within a single growing season. Climatic data suggest that dry conditions in the common garden as the summer progressed may have had a controlling influence on physiological trait responses. Characterizing genetically based phenotypic variation and how it contributes to clone vigor provides a critical link to understanding constraints to aspen viability in its western range.