Wing dimorphism occurs in insects as a survival strategy to adapt to environmental changes. In response to environmental cues, mother aphids transmit signals to their offspring, and the offspring either emerge as winged adults or develop as wingless adults with degeneration of the wing primordia in the early instar stage. However, how the wing morph is determined in the early instar stage is still unclear. Here, we established a surgical sampling method to obtain precise wing primordium tissues for transcriptome analysis. We identified Wnt as a regulator of wing determination in the early second instar stage in the pea aphid. Inhibiting Wnt signaling via knockdown of Wnt2, Wnt11b, the Wnt receptor-encoding gene fz2 or the downstream targets vg and omb resulted in a decreased proportion of winged aphids. Activation of Wnt signaling via knockdown of miR-8, an inhibitor of the Wnt/Wg pathway, led to an increased proportion of winged aphids. Furthermore, the wing primordia of wingless nymphs underwent apoptosis in the early second instar, and cell death was activated by knockdown of fz2 under the wing-inducing condition. These results indicate that the developmental plasticity of aphid wings is modulated by the intrinsic Wnt pathway in response to environmental challenges.