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Abstract Locomotor evolution in synapsids involved numerous functional shifts associated with the transition from sprawled to erect limb postures on the line to therian mammals. Given that bone structure frequently reflects functional requirements, this study investigated evolutionary changes in synapsid humerus and femur proportions as a lens to evaluate functional shifts through time. A total of 936 bones were measured, representing 330 species across the full 320+ million years of synapsid history. This dataset was used to test whether transformations in stylopod proportions are consistent with inferred changes in bone loading mechanics, alignment of joint and muscle forces, muscular control of the shoulder and hip, and differential support of body weight by the fore‐ and hindlimbs. As variation in bone dimensions may also correlate with bone or body size, this study first developed a novel approach for calculating species‐specific, size‐corrected measures of bone proportions. By disentangling the effect of body size from functional signals recorded in bone geometry, this then enabled a node‐to‐node appraisal of how bone allometry itself evolved through time. Ancestral state reconstruction of size‐corrected stylopod proportions reveals trends that broadly support many hypothesized shifts in locomotor biomechanics along the therian stem lineage. However, patterns of transformation are frequently complex, suggesting functional mosaicism, and stylopod proportions that typify therians as a whole are often not achieved until crown Theria itself. Several instances of temporary trend reversal are also inferred, particularly within non‐mammalian cynodonts, indicating greater functional or ecological diversification in this group.