Insects constitute the most diverse set of animals and the largest proportion of biomass on earth, and the majority of insect species undergo a soft-bodied larval stage. These soft-bodied organisms translocate using a variety of gaits, including burrowing, swimming, and crawling. Despite the ubiquity of soft-bodied animal life, studies of soft-bodied locomotion and biomechanics are under-represented in the literature. For example, caterpillars, which are soft-bodied, legged, terrestrial crawlers, have been studied extensively, and much has been learned about their physiology, life history, and morphology in the last century. Nonetheless, a decades-old hypothesis of the mechanism behind crawling, based primarily on observations of animal crawling in combination with inferences from anatomy, remains, for the most part, untested. In particular, this prevailing model of crawling lacks specific information on the biomechanics of the crawler’s body and how compliant materials like those of a soft-bodied crawler are controlled during a specific gait. Here, I examine several areas critical to the control of crawling in the Hawkmoth caterpillar, Manduca sexta. I begin with an examination of one of the more likely sources of sensory feedback during crawling, the Lepidopteron stretch receptor organ, which relays sensory information on segment length and stretch velocity. I present the result of efforts by myself and several collaborators to resolve the motor patterns generated in the larger of the longitudinal muscles in the Manduca abdomen during straight-line crawling. And, I present evidence for visceral-locomotory pistoning, a novel locomotory feature of caterpillar crawling wherein the gut moves back and forth within the hemocoel in coordination with the head and terminal segment but independently of the abdominal body wall, essentially decoupling the locomotory and alimentary systems. I examine these results in the context of the prevailing crawling hypothesis and show that the motor patterns we find in crawling caterpillars and the capabilities of the stretch receptor organ during crawling are inconsistent with the prevailing model. However, based on recent studies using ground reaction force data that have demonstrated that the crawling caterpillar generates compressive forces on the substrate on which it crawls – a so-called “environmental skeleton” – I assert that our findings do support an emerging hypothesis that the soft-bodied crawler generates propoulsive axial force using tension within its body and anchored by substrate compression. I re-examine the preceding crawling studies on motor coordination, sensory feedback, and tissue movements in the context of this new hypothesis, and offer examples of how a caterpillar with an environmental skeleton can employ this strategy, not only for straight-line crawling, but also for variations on crawling and non-crawling behaviors. Finally, I suggest that crawling Manduca sexta may offer a case study in morphological embodiment, an idea that organically generates several new avenues of exploration, both into the unknown and possibly more complex properties of a compliant body and into how such properties may simplify the computational complexity of the problem of crawling for a relatively simple soft-bodied organism like Manduca sexta.