Many traits show canalization (robustness against genetic or environmental perturbation). But it’s unclear how the buffering of a developmental process may be affected if adaptive evolution changes its phenotypic outcome. Highland Ethiopian D. melanogaster have evolved the largest thorax and wing length of any natural population. This size evolution is facilitated by an evolutionary tradeoff in which flies lay fewer but larger eggs, and it involves increases in both cell proliferation and somatic ploidy. Motivated by an unexpected frequency of wing vein abnormalities in Ethiopian inbred lines, we hypothesized that wing size evolution was accompanied by decanalized wing development in these flies. We repurposed a classic forward genetic approach (chemical mutagenesis) to test whether Ethiopian strains’ wing development was more susceptible to genetic perturbation than a small-winged low altitude population (Zambia). Indeed, the offspring of mutagenized Ethiopian flies showed much higher rates of novel wing abnormalities, demonstrating reduced genetic robustness. Furthermore, wing size and decanalization cosegregated in the advanced generation offspring of a cross between Ethiopia and Zambia strains, implying that wing size variants undermined developmental buffering. Our results constitute the first natural example of a tissue’s morphological evolution being associated with decanalized development, suggesting that decanalization might reflect an important cost of adaptation.