After adopting primarily underground lifestyles, 3 independent lineages of subterranean mammals – the naked mole rat, star-nosed mole, and cape golden mole – evolved greatly reduced eyesight in a process known as regressive evolution. The multiple independent cases of regressive evolution allow an investigation of genomic patterns underlying this phenotypic convergence. Using new phylogenomic methods we found that hundreds of genes show increased evolutionary rates specifically in subterranean species, primarily due to a loss of functional constraint. These genes were predominantly involved in eye physiology, such as those encoding lens crystallins, photoreceptors and transduction pathways. Furthermore, bright-light color photoreceptors were clearly more degraded than dim-light receptors indicating they were lost earlier during regression. This finding suggests these species underwent a gradual transition to the subterranean environment, retaining vision in dim light for longer. Regressive evolution proceeded very differently between eye tissues; while lens and retinal genes are highly degraded, corneal genes remain under constraint, perhaps because they continue to provide a protective outer barrier for the vestigial eye. Moreover, genes important for the embryological development of all eye tissues remain highly conserved, potentially because they are expressed during the development of tissues outside the eye. For example, the coding portion of PAX6, a key transcription factor in the development of eye and the central nervous system, showed no signs of regression in subterranean mammals. We also explore an alternative explanation that development of early embryonic eye tissues is important for the canalized development of neighboring tissues such as the brain. Observed developmental patterns in these species are consistent with this hypothesis. In contrast to its coding sequence, we found that PAX6’s eye-specific enhancers were evolving at a much faster rate in subterranean species, likely due to relaxed constraint, relative to aboveground species. PAX6’s enhancers active in other tissues did not demonstrate this pattern. This observation led us to perform a genome-wide screen to identify 40 new candidate eye-specific cis-regulatory sequences, which clustered near confirmed eye development genes. Thus, the results of convergent, regressive evolution provide a powerful means to assign functions to uncharacterized elements in the genome. We conclude that eye-related genes and regulatory elements show convergent patterns of loss and retention during repeated instances of regressive evolution, and that regression occurs differentially across tissues, physiology and development.