During metamorphosis of the hawkmoth, Manduca sexta, the muscles, cuticular structures, and most sensory neurons of the larval thoracic legs are replaced by new elements in the adult legs. The thoracic leg motoneurons, however, survive the loss of the larval muscles and persist to innervate new targets in the imaginal legs. Here we have used biocytin staining, immunocytochemistry, and confocal microscopy to follow the fates of the peripheral processes and presynaptic terminals of the leg motoneurons. Although the most distal processes of the motor nerves retract following the degeneration of larval leg muscles, the axon terminals always retain close association with the muscle remnants and the anlagen of the new adult muscles. As the imaginal muscles differentiate and enlarge, the motor terminals expand to form adult presynaptic terminals. An antibody to the presynaptic protein, synaptotagmin, revealed its localization to the terminal varicosities in both larval and adult stages but distribution within pre-terminal branches during adult development. Electrophysiological methods revealed that functional neuromuscular transmission first occurs quite early during metamorphosis, before the differentiation of contractile elements in the muscle fibers.