The New World family Didelphidae, the basal lineage within marsupials, is commonly viewed as morphologically conservative, yet includes aquatic, terrestrial, scansorial, and arboreal species. Here, I quantitatively estimated the existing variability in size and shape of the Didelphidae scapula (1076 specimens from 56 species) using geometric morphometrics, and compared size and shape differences to evolutionary and ecologic distances. I found considerable variation in the scapula morphology, most of it related to size differences between species. This results in morphologic divergence between different locomotor habits in larger species (resulting from increased mechanical loads), but most smaller species present similarly shaped scapulae. The only exceptions are the water opossum and the short-tailed opossums, and the functional explanations for these differences remain unclear. Scapula size and shape were mapped onto a molecular phylogeny for 32 selected taxa and ancestral size and shapes were reconstructed using squared-changed parsimony. Results indicate that the Didelphidae evolved from a medium- to small-sized ancestor with a generalized scapula, slightly more similar to arboreal ones, but strikingly different from big-bodied present arboreal species, suggesting that the ancestral Didelphidae was a small scansorial animal with no particular adaptations for arboreal or terrestrial habits, and these specializations evolved only in larger-bodied clades.