Signals from individual rod photoreceptors are conveyed through a highly conserved pathway in the mammalian retina called the rod bipolar pathway. In this pathway rod outputs are pooled by a rod ON bipolar cell (ON-BC), which in turn are pooled by a depolarizing AII amacrine cell and relayed through cone photoreceptor circuits to the retinal output, the ganglion cells. The depolarizing light-evoked responses of rod ON-BCs are generated by a metabotropic-signaling cascade involving the glutamate receptor, mGluR6, the heterotrimeric G protein, Gao, and the cationic channel, TRPM1. The time course of signaling via heterotrimeric G proteins is controlled through their activation by G-protein coupled receptors and deactivation through the action of GTPase accelerating proteins (GAPs). In retinal ON-BCs the rate of intrinsic spontaneous hydrolysis of GTP by Gao is very slow, and GAP activity is required to initiate the fast depolarizing light response. However, the identity of the dominant GAP in these cells has not been known. Using single- cell recordings we showed that the elimination of RGS7 did not influence dark-adapted light-evoked responses, but the concurrent elimination of RGS11 severely reduced their magnitude and dramatically slowed response onset. In RGS7/RGS11 double-knockout mice, light-evoked responses were only observed during persistent activation of rod photoreceptors with stimuli that saturate rods. These results suggest that RGS7 and RGS11 together provide the dominant GAP in the mGluR6 signaling cascade that is essential for setting the sensitivity and temporal resolution in the ON-BCs of the rod bipolar pathway.