Many tropical fruit-feeding nymphalid butterflies are associated with either the forest canopy or the understory, however, the exceptions offer insights into the origins of tropical diversity. As it occurs in both habitats of tropical forests in Ecuador and Peru, Archaeoprepona demophon is one such exception. We compared patterns of occurrence of A. demophon in the canopy and understory and population genomic variation for evidence of ecological and genetic differentiation between habitats. We found that butterfly occurrences in the canopy were largely uncorrelated with occurrences in the understory at both localities, indicating independent demographic patterns in the two habitats. We also documented modest, significant genome-level differentiation at both localities. Genetic differentiation between habitat types (approximately 20m in elevation) were comparable to levels of differentiation between sampling locations (approximately 1500km). We conclude that canopy and understory populations of A. demophon represent incipient independent evolutionary units. These findings support the hypothesis that divergence between canopy and understory-associated populations might be a mechanism generating insect diversity in the tropics.