Several aspects of leg development in the moth Manduca sexta were examined using the homeotic mutation Octopod (Octo). This mutation causes a transformation of the ventral epidermis of the first abdominal segment (A1) to that of the third thoracic segment (T3), resulting in the presence of thoracic-like legs on A1. The degree of transformation of A1 is variable, ranging from bumps on the cuticle to fully segmented thoracic-like legs. In the normal thoracic legs, clusters of undifferentiated cells known as differentiation centers are located around the coxal-trochanteral, femoral-tibial, and tibial-tarsal joints. The adult thoracic legs develop from the differentiation centers at metamorphosis. The homeotic legs of the Octopod larvae also have differentiation centers at comparable positions in the homeotic leg. As a result, the number of leg segments in a mutant adult is correlated with the number of segments and differentiation centers that animal had in its larval homeotic leg. Our data suggest that the differentiation center located at the coxal-trochanteral joint forms the adult coxa and trochanter, the center at the larval femoral-tibial joint the adult femur and tibia, and the differentiation center at the larval tibial-tarsal joint the adult tarsus. Homeotic larval legs which include at least a femur have supernumerary muscles, while adult homeotic legs rarely show discrete muscle. The homeotic larval muscles appear to have thoracic identities, based on their attachment points and the timing of their degeneration at the larval-pupal transition. They are innervated by a motoneuron that is normally present in A1 where it innervates the ventral lateral external muscle (VLE). In mutant animals, the same motoneuron innervates all of the homeotic muscles and the VLE. We consider possible mechanisms underlying the development of homeotic muscles and their innervation. At the larval-pupal transition, the VLE in mutant animals degenerates at its normal time, which is 3 days after the degeneration of the homeotic muscles. Thus, despite their common innervation, the two muscle types degenerate according to their own schedules, indicating that the developmental fates of the muscles are not dictated by their innervating neuron but are intrinsic to the muscles themselves.