In daylight, demand for visual chromophore (11-cis-retinal) exceeds supply by the classical visual cycle. This shortfall is compensated, in part, by the retinal G-protein-coupled receptor (RGR) photoisomerase, which is expressed in both the retinal pigment epithelium (RPE) and in Müller cells. The relative contributions of these two cellular pools of RGR to the maintenance of photoreceptor light responses are not known. Here, we use a cell-specific gene reactivation approach to elucidate the kinetics of RGR-mediated recovery of photoreceptor responses following light exposure. Electroretinographic measurements in mice with RGR expression limited to either cell type reveal that the RPE and a specialized subset of Müller glia contribute both to scotopic and photopic function. We demonstrate that 11-cis-retinal formed through photoisomerization is rapidly hydrolyzed, consistent with its role in a rapid visual pigment regeneration process. Our study shows that RGR provides a pan-retinal sink for all-trans-retinal released under sustained light conditions and supports rapid chromophore regeneration through the photic visual cycle. Display omitted •RGR supports rapid photoproduction of the visual chromophore•A subpopulation of Müller glia exhibits specialization in supporting the photic visual cycle•RPE and Müller glia RGR pools contribute to cone visual pigment recycling•RGR accelerates rod dark adaptation upon the transition from bright light to darkness Tworak et al. report that the RGR-mediated photic visual cycle found in the retinal pigment epithelium and in specialized Müller glia in the mammalian retina constitutes a fast visual-pigment recycling pathway that modulates both cone function in bright light and rod dark adaptation upon the transition to darkness.