Eyes have evolved numerous times with a great diversity of forms, yet little is known about how eye gain and loss is related to photic environment. The pteriomorphian bivalves (e.g., oysters, scallops, and ark clams) display a remarkable range of photoreceptor organs and ecologies, making them a suitable system to investigate the association between eye evolution and ecological shifts. The present phylogenetic framework was based on amino acid sequences from transcriptome datasets and nucleotide sequences of five additional genes. In total, 197 species comprising 22 families from all five pteriomorphian orders were examined, representing the greatest taxonomic sampling to date. Morphological data were acquired for 162 species and lifestyles were compiled from the literature. Photoreceptor organs occur in 11 families and have arisen exclusively in epifaunal lineages, that is, living above the substrate, at least five times independently. Models for trait evolution consistently recovered higher rates of loss over gain. Transitions to crevice-dwelling habit appear associated with convergent gains of eyespots in some epifaunal lineages. Once photoreceptor organs have arisen, multiple losses occurred in lineages that shift to burrowing lifestyles and deep-sea habitats. The observed patterns provide a basis for future investigations focusing on the diversification of photoreception in bivalve molluscs and the potential ecological factors affecting eye evolution.