A key focus of evolutionary developmental biology is on how phenotypic diversity is generated. In particular, both plasticity and developmental instability can contribute to phenotypic variation among genetically identical individuals, but the interactions between the two phenomena and their general fitness impacts are unclear. We discovered a striking example of asymmetry in pea aphids: the presence of wings on one side and the complete or partial absence of wings on the opposite side. We used this asymmetric phenotype to study the connection between plasticity, developmental instability, and fitness. We found that this asymmetry equally affects both sides and thus is a developmental instability; is present in some genetically unique lines but not others and thus has a genetic basis; and has intermediate levels of fecundity, and thus does not necessarily have negative fitness consequences. We conclude that this dramatic asymmetry may arise from incomplete switching between developmental targets, linking plasticity and developmental instability. We posit that what we have observed may be a more widespread phenomenon, occurring across species that routinely produce distinct, alternative phenotypes.