Understanding how organismal design evolves in response to environmental challenges is a central goal of evolutionary biology. In particular, assessing the extent to which environmental requirements drive general design features among distantly related groups is a major research question. The visual system is a critical sensory apparatus that evolves in response to changing light regimes. In vertebrates, the optic tectum is the primary visual processing center of the brain, and yet it is unclear how, or whether this structure evolves while lineages adapt to changes in photic environment. On one hand, dim‐light adaptation is associated with larger eyes and enhanced light‐gathering power that could require larger information processing capacity. On the other hand, dim‐light vision may evolve to maximize light sensitivity at the cost of acuity and color sensitivity, which could require less processing power. Here, we use X‐ray microtomography and phylogenetic comparative methods to examine the relationships between diel activity pattern, optic morphology, trophic guild, and investment in the optic tectum across the largest radiation of vertebrates—teleost fishes. We find that despite driving the evolution of larger eyes, enhancement of the capacity for dim‐light vision generally is accompanied by a decrease in investment in the optic tectum. These findings underscore the importance of considering diel activity patterns in comparative studies and demonstrate how vision plays a role in brain evolution, illuminating common design principles of the vertebrate visual system.