There is abundant theoretical and empirical evidence for the influence of variational properties of populations on microevolution, and more limited support for their lasting impact during macroevolution. This study applies evolutionary quantitative genetic approaches to assess the long-term impact of within-population phenotypic variation and covariation (the P matrix) on population divergence in recent humans and species diversification in genus Homo. Similarity between the primary axes of within- and between-population craniofacial variation confirms a role for pmax in human population divergence, although diversification is not constrained to be unidimensional. The long term impact of the P matrix on craniofacial evolution is supported by higher-than-average evolvabilities along most branches of the Homo tree, but statistical uncertainty inherent in the data reduce confidence in this conclusion. Higher evolvability is not statistically correlated with increased rate of evolution, although the relationship is in the predicted direction. This is due in part to the high evolutionary rate on the early modern human branch despite its moderate level of evolvability. There was evidence for neutral evolution as well as directional and stabilizing selection over the Plio-Pleistocene using generalized genetic distance as a test statistic.