Phototransduction in flies is the fastest known G protein-coupled signaling cascade, but how this performance is achieved remains unclear. Here, we investigate the mechanism and role of rhodopsin inactivation. We determined the lifetime of activated rhodopsin (metarhodopsin = M*) in whole-cell recordings from Drosophila photoreceptors by measuring the time window within which inactivating M* by photoreisomerization to rhodopsin could suppress responses to prior illumination. M* was inactivated rapidly (τ ∼20 ms) under control conditions, but ∼10-fold more slowly in Ca2+-free solutions. This pronounced Ca2+ dependence of M* inactivation was unaffected by mutations affecting phosphorylation of rhodopsin or arrestin but was abolished in mutants of calmodulin (CaM) or the CaM-binding myosin III, NINAC. This suggests a mechanism whereby Ca2+ influx acting via CaM and NINAC accelerates the binding of arrestin to M*. Our results indicate that this strategy promotes quantum efficiency, temporal resolution, and fidelity of visual signaling.