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The ‘sprawling–parasagittal’ transition was a major postural shift during mammal evolution, but ‘when’ and ‘how’ it occurred has been debated for decades. Previous work focused on a few exceptional fossils from discrete points in time, but broader studies of individual limb elements may provide a more comprehensive evolutionary perspective. Here we address when and how parasagittal forelimb posture evolved in the ancestors of mammals, the non-mammalian synapsids (NMS), using functional adaptive landscape analysis of the humerus bone, incorporating data from morphology, function, and phylogeny, to assess forelimb evolution in deep time. The humerus is subjected to different functional stresses in parasagittal vs. sprawling limbs, and so its morphology is expected to reflect postural differences. We measured humerus shape and various functional traits on a large sample of NMS (n = 61), with a diverse array of extant taxa (n = 140) serving as a robust comparative dataset. We recover distinct adaptive landscapes for extant sprawling and parasagittal taxa, highlighting functional specialization of the humerus associated with different postures. The landscapes for NMS had distinct adaptive peaks from extant sprawlers. While there is repeated evolution of humeri representing ‘transitional’ postures in NMS, humeri consistent with parasagittal posture do not appear until the crown group. Our data reveal the complexity of postural evolution within Synapsida, with the ‘sprawling-parasagittal’ transition typified by considerable homoplasy, and postural variation within individual synapsid clades.