Drosophila melanogaster photoreceptor cells are capable of detecting single photons. This utmost sensitivity is critically dependent on the maintenance of an exceedingly low, dark, spontaneous activity of photoreceptor cells. However, the underlying mechanisms of this hallmark of phototransduction are not fully understood. An analysis of the Drosophila visual heterotrimeric (αβγ) Gq protein revealed that wild-type Drosophila flies have about a twofold excess of Gβ over Gα subunits of the visual Gq protein. Studies of Gβe mutants in which the excess of Gβ was genetically eliminated showed dramatic dark, spontaneous activity of the photoreceptor cells, whereas concurrent genetic reduction of the Gα subunit, which restored the excess of Gβ, abolished this effect. These results indicate that an excess of Gβ over Gα is a strategy used in vivo for the suppression of spontaneous activity, thereby yielding a high signal to noise ratio, which is characteristic of the photoreceptor light response. This mechanism could be relevant to the regulation of G protein signaling in general.