Rhabdomeric Opsins (r-Opsins) serve as light-sensory molecules in cephalic eye photoreceptors of many invertebrates, but also play roles in additional sensory organs. This has prompted questions on the evolutionary relationship of the cell types, specifically if ancient r-Opsins cells possessed non-photosensory functions. By extracting and profiling cephalic and non-cephalic r-opsin1-expressing cell types of the marine bristleworm Platynereis dumerilii, we find evidence for shared and distinct identities between these two cell types. We establish that non-cephalic cells possess a mechanosensory signature, but also a full set of phototransduction components. Using cell-culture-based second messenger assays, we determine that Platynereis r-Opsin1 is a Gα_q-coupled blue-light receptor. Profiling of cells in r-opsin1 mutant animals, and comparing cells under dim and bright light conditions reveals that in the non-cephalic cell type, light – mediated by r-Opsin1 – adjusts the expression level of a calcium transporter relevant for auditory mechanosensation in vertebrates. We finally establish a supervised, deep learning-based quantitative behavioral analysis pipeline to assess animal trunk movements. We identify light-dependent differences in the fine-tuning of the worms’ undulatory movements in mutant vs. wildtype headless trunks, which are known to require mechanosensory feedback. Altogether, our results provide support for an evolutionary concept in which r-Opsins act as ancient, light-dependent modulators of mechanosensation. Our findings refine the reconstruction of sensory cell type evolution, and suggest that light-independent mechanosensory roles of r-Opsins likely result from secondary evolutionary processes.