TRP and TRPL are two light-sensitive cation channel subunits required for the Drosophila photoresponse; however, our understanding of the identities, subunit composition, and function of the light-responsive channels is incomplete. To explain the residual photoresponse that remains in the trp mutant, a third TRP-related subunit has previously been proposed to function with TRPL. Here, we identify such a subunit, TRPγ. We show that TRPγ is highly enriched in photoreceptor cells and preferentially heteromultimerizes with TRPL in vitro and in vivo. The N-terminal domain of TRPγ dominantly suppressed the TRPL-dependent photoresponse, indicating that TRPγ-TRPL heteromultimers contribute to the photoresponse. While TRPL and TRPγ homomultimers are constitutively active, we demonstrate that TRPL-TRPγ heteromultimers form a regulated phospholipase C-(PLC-) stimulated channel.