Author Summary Animals sense light through receptors called Rhodopsins. These proteins are typically localized to stacked membranes in photoreceptors. In flies, upon light exposure, Rhodopsin undergoes conformational changes and becomes active as metarhodopsin. Metarhodopsin then initiates a signaling cascade that activates the photoreceptor cell. To deactivate the light response, metarhodopsin is converted back into Rhodopsin by absorption of another photon of light. Under certain conditions, metarhodopsin cannot be converted back to Rhodopsin, and it is then endocytosed and degraded. Rhodopsin then needs to be synthesized and delivered back to the membrane stacks. Here, we show that the Calmodulin-binding protein Crag is required for the delivery of newly made Rhodopsin to the membrane stacks. Loss of Crag leads to the accumulation of Rhodopsin in the cytosol, followed by shrinkage of membrane stack volume, and, eventually, photoreceptor cell degeneration. We also show that Crag activates a target protein, Rab11, which mediates the vesicular transport of Rhodospin to the membrane. Finally, we document that the human homolog of Crag, DENND4A, is able to rescue the loss of Crag in flies, suggesting that DENND4A functions in a similar process in vertebrates.