The striking structural variation seen in arthropod visual systems can be explained by the overall quantity and spatio-temporal structure of light within habitats coupled with developmental and physiological constraints. However, little is currently known about how fine-scale variation in visual structures arise across shorter evolutionary and ecological scales. In this study, we characterise patterns of interspecific (between species), intraspecific (between sexes) and intraindividual (between eye regions) variation in the visual system of four ithomiine butterfly species. These species are part of a diverse 26-Myr-old Neotropical radiation where changes in mimetic colouration are associated with fine-scale shifts in ecology, such as microhabitat preference. By using a combination of selection analyses on visual opsin sequences, in-vivo ophthalmoscopy, micro-computed tomography (micro-CT), immunohistochemistry, confocal microscopy, and neural tracing, we quantify and describe physiological, anatomical, and molecular traits involved in visual processing. Using these data, we provide evidence of substantial variation within the visual systems of Ithomiini, including: i) relaxed selection on visual opsins, perhaps mediated by habitat preference, ii) interspecific shifts in visual system physiology and anatomy, and iii) extensive sexual dimorphism, including the complete absence of a butterfly-specific optic neuropil in the males of some species. We conclude that considerable visual system variation can exist within diverse insect radiations, hinting at the evolutionary lability of these systems to rapidly develop specialisations to distinct visual ecologies, with selection acting at both the perceptual, processing, and molecular level.