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Nervous systems evolve to adapt an animal’s behavior to its ecological niche, but the specific genetic and cellular changes underlying this process are poorly understood. We have compared the olfactory circuits of the specialist fly species Drosophila sechellia, which feeds and breeds exclusively on the acid-rich fruit of Morinda citrifolia, with its generalist cousins D. melanogaster and D. simulans, which are associated with a wide range of fermenting fruits. We have identified both loss and gain of sensory responses to acids in D. sechellia and link these to single nucleotide differences within a tandem cluster of olfactory receptor genes. Peripheral functional differences are accompanied by regulatory and developmental modifications that shape the species-specific neuroanatomical organization of acid-sensing pathways. These traits can explain the distinct preferences of these species toward important odor cues in the environment, thereby linking chemosensory ecology to adaptive genetic changes influencing nervous system structure and function.