d-Cysteinolic acid is a prominent sulfur-containing compound in marine and freshwater ecosystems, yet its metabolic fate has remained largely uncharacterized. Here, we describe a newly identified d-cysteinolic acid degradation pathway in a marine model bacterium Ruegeria pomeroyi DSS-3. This pathway involves a PLP-dependent cysteinolic acid racemase (ClaA) that interconverts d- and l-cysteinolic acids, followed by a NAD+-dependent l-cysteinolic acid dehydrogenase (ClaB) that oxidizes l-cysteinolic acid to l-cysteate. A cysteate racemase (CuyB) then converts l-cysteate to d-cysteate, the preferred substrate for the sulfolyase CuyA. Bioinformatic analysis of the Tara Oceans gene atlas reveals that ClaA and CuyA homologues are widespread in marine bacterial populations, particularly within the alphaproteobacterial Roseobacter and SAR116 groups and the gammaproteobacterial SUP05 clade. Relative abundance of gene homologues correlates with surface water chlorophyll levels, linking d-cysteinolic acid degradation to photosynthetic primary production. This discovery advances our understanding of marine sulfur cycling and highlights d-cysteinolic acid as an important metabolic currency in microbial networks.