Most cellular organisms respond to light. In animals, the phototransduction system has evolved from localised light-detecting photoreceptors to ultimately complex eyes and vision. Here, we investigate the origin of metazoan photodetection and transduction by comparing well-characterised opsin-based photosystems in neural animals with those in the sponge Amphimedon queenslandica. Although sponges lack neurons and opsin genes, they can respond rapidly to light. In Amphimedon larva, this is guided by the light-sensing posterior pigment ring. We first use cell type-specific transcriptomes to reveal that genes that characterise eumetazoan Gt- and Go-mediated photosystems are enriched in the Amphimedon pigment ring. We then apply a suite of cell signalling pathway agonists and antagonists to swimming larvae exposed to directional light. These experiments implicate metabotropic glutamate receptors, phospholipase-C, protein kinase C and voltage-gated calcium channel in larval phototaxis. We find that U-73122-inhibition of phospholipase-C, a key transducer of the Gq-mediated pathway, completely reverses phototactic behaviour. Together, these results are consistent with aneural sponges sharing with neural metazoans an ancestral set of signal transduction pathways that have been maintained in these disparate photosensory systems since the last common animal ancestor.