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ABSTRACT Lateralization of neuronal functions plays a critical role in regulating behavioral flexibility, but the underlying molecular mechanisms are challenging to establish at a single-neuron level. We previously showed that attraction ofC. elegansto a medium-chain alcohol switches to avoidance in a uniform background of a second attractive odorant. This context-dependent behavioral plasticity is mediated by symmetric inversion of the odor-evoked response sign in the bilateral AWC olfactory neurons. Here we show that this symmetric response plasticity is driven by asymmetric molecular mechanisms in the AWC neuron pair. Mutations in thegcy-12receptor guanylyl cyclase abolish odor response plasticity only in AWC^OFF; the opposing odor-evoked response signs in AWC^OFFand AWC^ONingcy-12mutants results in these animals being behaviorally indifferent to this chemical. We find thatgcy-12is expressed, and required, in both AWC neurons to regulate odor response plasticity only in AWC^OFF. We further show that disruption of AWC fate lateralization results in loss of asymmetry in the response plasticity ingcy-12mutants. Our results indicate that symmetric neuronal response plasticity can arise from asymmetry in underlying molecular mechanisms, and suggest that lateralization of signaling pathways in defined conditions may enhance neuronal and behavioral flexibility.