Little is known about when, how or even if the wing development gene network elucidated in Drosophila is deployed in direct-developing insects. Here we identify the wing development genes (as determined in Drosophila) of the pea aphid (Acyrthosiphon pisum), which produces winged or unwinged adults in response to environmental cues. We find that the principal wing development genes studied in Drosophila are present in the aphid genome and that apterous and decapentaplegic exhibit duplications. We followed expression levels of 11 of these developmental genes at embryogenesis and across the nymphal instars. Six showed significant stage-specific expression level effects and apterous1 exhibited significantly different expression levels between winged and unwinged morphs, suggesting this gene acts proximately to realize polyphenic development.