Bivalve molluscs synthesize remarkably complex shells from calcium carbonate and an organic matrix of proteins secreted from the dorsal edge of the mantle. Molecular analyses of shell matrix proteins (SMPs) have suggested high rates of gene turnover despite the conserved nature of the shell itself. Here, we used proteomic and transcriptomic data to identify the SMPs and other biomineralization proteins from seven bivalve species that diverged 3-513 Mya. Contrary to previous studies that identified only a few shared biomineralization transcripts across the Bivalvia, we found 83 that were ubiquitous, all validated by proteomic analysis. 46 of these candidates are homologous to annotated genes with functions central to shell deposition, including interacting with polysaccharides, forming extracellular matrix, inhibiting proteases, and binding calcium. These shell-associated proteins mark a 20-fold increase in the size of the bivalve biomineralization toolbox. Our results suggest that bivalve biomineralization is underpinned by a conserved suite of many genes and call into question the need to invoke high levels of novel gene recruitment to explain the evolution of SMP diversity.