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Diaphyseal cross-sectional geometry (CSG) is an effective indicator of humeral bilateral asymmetry. However, previous studies primarily focused on CSG properties from limited locations to represent the overall bilateral biomechanical performance of humeral diaphysis. In this study, the complete humeral diaphyses of 40 pairs of humeri from three Chinese archaeological populations were scanned using high-resolution micro-CT, and their biomechanical asymmetries were quantified by morphometric mapping. Patterns of humeral asymmetry were compared between sub-groups defined by sex and population, and the representativeness of torsional rigidity asymmetry at the 35% and 50% cross-sections (J35 and J50 asymmetry) was testified. Inter-group differences were observed on the mean morphometric maps, but were not statistically significant. Analogous distribution patterns of highly asymmetrical regions, which correspond to major muscle attachments, were observed across nearly all the sexes and populations. The diaphyseal regions with high variability of bilateral asymmetry tended to present a low asymmetrical level. The J35 and J50 asymmetry were related to the overall humeral asymmetry, but the correlation was moderate and they could not reflect localized asymmetrical features across the diaphysis. This study suggests that the overall asymmetry pattern of humeral diaphysis is more complicated than previously revealed by individual sections.