A uniquely female behavior in grasshoppers, oviposition, is driven by neural circuitry in the terminal abdominal segments of the female's central nervous system. Because it is known that the embryonic pattern of neuroblasts is sexually monomorphic in these animals, we were interested to know how the central nervous system of adults is organized to support the obvious behavioral dimorphism. Here, we compare three classes of identifiable adult neurons: ovipositor motor neurons, efferent dorsal unpaired median (DUM) neurons, and DUM interneurons in the eighth abdominal neuromere. Cobalt backfills of the eighth tergal nerves revealed identical complements of motor neurons in males and females. Included among these neurons in the male were putative homologues of two sets of ovipositor muscle motor neurons. Whereas these motor neurons supply two ovipositor muscles in the female, they are divided to supply three muscles in males. The eighth abdominal neuromere of both sexes contained seven efferent DUM neurons, but peripheral axon projections varied between males and females in accordance with gender-specific targets. In the eighth neuromere of females, some 22 small cell bodies of DUM interneurons were stained with Toluidine blue, whereas only three male DUM interneurons were found. Male muscle homologues were induced to express a rhythmical motor pattern by experimental methods that activate the oviposition pattern in females. The induced pattern in males is of unknown behavioral significance. Although oviposition normally occurs only after sexual maturity, the motor pattern could be activated at all life stages in females, including embryos, as early as 90% of embryonic development.