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CO2sensation represents an interesting example of nervous system and behavioral evolutionary divergence. The underlying molecular mechanisms, however, are not understood. Loss ofmicroRNA-279inDrosophila melanogasterleads to the formation of a CO2sensory system partly similar to the one of mosquitoes. Here, we show that a novel allele of the pleiotropic transcription factor Prospero resembles themiR-279phenotype. We use a combination of genetics andin vitroandin vivoanalysis to demonstrate that Pros participates in the regulation ofmiR-279expression, and that reexpression ofmiR-279rescues theprosCO2neuron phenotype. We identify common target molecules ofmiR-279and Pros in bioinformatics analysis, and show that overexpression of the transcription factors Nerfin-1 and Escargot (Esg) is sufficient to induce formation of CO2neurons on maxillary palps. Our results suggest that Prospero restricts CO2neuron formation indirectly viamiR-279and directly by repressing the shared target molecules, Nerfin-1 and Esg, during olfactory system development. Given the important role of Pros in differentiation of the nervous system, we anticipate that miR-mediated signal tuning represents a powerful method for olfactory sensory system diversification during evolution.