Understanding among and within population genetic variation of ecologically important plant traits provides insight into the potential evolutionary processes affecting those traits. The strength and consistency of selection driving variability in traits would be affected by plasticity in differences among genotypes across environments (G x E). We investigated population divergence, selection and environmental plasticity of foliar plant secondary metabolites (PSMs) in a dominant tree species, <i>Eucalyptus globulus</i>. Using two common garden trials we examined variation in PSMs at multiple genetic scales; among 12 populations covering the full geographic range of the species and among up to 60 families within populations. Significant genetic variation in the expression of many PSMs resides both among and within populations of <i>E. globulus</i> with moderate (e.g., sideroxylonal A h<sup>2</sup>op = 0.24) to high (e.g., macrocarpal G h<sup>2E. globulus, and identifies the formylated phloroglucinol compounds (particularly sideroxylonal) and a dominant oil, 1,8-cineole, as candidates for traits whose genetic architecture has been shaped by divergent selection. Additionally, as the genetic differences in these PSMs that influence community phenotypes is stable across environments, the role of plant genotype in structuring communities is strengthened and these genotypic differences may be relatively stable under global environmental changes.</sup>