While reducing the investment in the visual system of nocturnal/cave-dwelling species appears to be an evolutionarily stable strategy in response to the difficulty of locating food in the dark, relying on visual information for diurnal species is crucial for their survival and reproduction. However, the manner in which species evolve and adapt to the energetic demands placed upon them by environmental changes is not perfectly understood. In particular, if life in the dark is associated with a reduction in energetic demand, would relocation to a well-lit environment increase energetic demand? This question has a bearing upon our understanding of factors that influence the ability of species to adapt to new habitats. After observing that a sub-population of “Dark-flies” (i.e., fruit flies bred in the dark for more than 60 years) has been selected with a larger visual system (optic lobes) and brain over the course of being maintained in normal lighting conditions for 3 years (DF<sub>Light</sub>), we used the CAFÉ assay method to investigate the differences in the two strains’ energetic demands in the present study. We therefore measured brain size, body size, and food consumption in Dark-flies, DF<sub>Light</sub>, and Oregon flies (i.e., the fly species most genetically similar to Dark-flies). We found that the DF<sub>Light</sub> consumed more food solution than the Dark-flies, which correlates with that strain’s larger brain size and improved visual capability compared to the Dark-flies. In addition, and although the Oregon flies initially consumed less food solution than the DF<sub>Light</sub>, the amount consumed by these two strains by the end of the CAFÉ assay was approximately the same. This suggests that the Dark-flies have adapted their metabolism or feeding strategies in response to a dark environment. Our investigation therefore provides empirical evidence elucidating the manner in which energetic demands change in response to environmental changes and the cross-generational effect upon sensory-system investment.