Transient receptor potential (TRP) channels across species are expressed in sensory receptor cells, and often localized to specialized subcellular sites. In Drosophila photoreceptors, TRP-like (TRPL) channels are localized to the signaling compartment, the rhabdomere, in the dark, and undergo light-induced translocation into the cell body as a mechanism for long-term light-adaptation. We show that translocation of TRPL channels occurs in two distinct stages, first to the neighboring stalk membrane then to the basolateral membrane. In the first stage, light-induced translocation occurs within 5 minutes, whereas the second stage takes over 6 hours. The exclusive apical localization of TRPL channels in the first stage of translocation suggests that channels are released from the rhabdomere and diffuse laterally through the membrane into the adjoining stalk membrane. In the second stage, TRPL channels are localized in the basolateral membrane, implicating a different transport mechanism. Genetic analyses suggest that activation of the other light-activated TRP channel and eye-protein-kinase C (eye-PKC) are both required for the second stage of TRPL translocation in R1 to R6 photoreceptor cells, whereas only phospholipase C (PLC) is required for the first stage. Finally, we show that arrestin2 is required for the rhabdomeric localization and stability of TRPL channels.