Although many organisms experience relatively predictable environmental conditions throughout development, others, as a result of ontogenetic changes, inhabit very different environments across life stages, requiring them to navigate into habitats or microhabitats that they have not previously encountered. For holometabolous insects, late instars must often locate a safe site before undergoing pupation. In Lepidoptera, many pre-pupae cease feeding and wander in search of an appropriate pupation site; their preferences display a shift in behavioral responses to habitat-specific environmental cues, relative to those of feeding larvae. Having previously determined that pre-pupae of Epargyreus clarus (Cramer) (Lepidoptera: Hesperiidae) move from their Fabaceae host plant down into the leaf litter, where they construct a pupal refuge out of dried leaves and silk, we investigated the sensory cues used by E. clarus in selecting a pupation location. We further explored how responses to these cues vary between actively feeding larvae and non-feeding pre-pupae, both for individual insects and for stage-based cohorts. Using Y-tube assays, we determined that pre-pupae used visual (light) and gravitational cues to move from host plants into the leaf litter, whereas the odor cues we tested did not appear to influence their decision-making. Directional responses to both light and gravity reversed over ontogeny, allowing the two life stages to make use of the same cues to produce stage-appropriate adaptive behaviors.