Schistosoma mansoni parasites inhabit three distinct environments including water, intermediate molluscan hosts, and definitive vertebrate hosts. Determining how schistosomes interact with these environments may be one mechanism by which suitable vaccines or novel chemotherapeutic targets will be identified. Towards this end, we describe the identification of a 36-kDa S. mansoni protein that shares extensive sequence similarity to light absorbing rhodopsin guanine protein coupled receptors (GPCRs). This protein, S. mansoni rhodopsin (SmRHO), is the first molecularly characterized GPCR described in schistosomes. Sequence analysis reveals that SmRHO shares extensive phylogenetic conservation among rhodopsins/opsins expressed in water-dwelling invertebrates, possibly indicative of orthology. We demonstrate here that SmRHO is expressed in the free-living, light responsive miracidia and cercaria stages and is down-regulated in the adult, vertebrate residing forms. Moreover, we show that SmRHO is localized to sub-tegumental structures found towards the anterior end of cercariae. As SmRHO may be implicated in schistosome photoreception processes, we have begun a search for additional parasite encoded GPCR super-family members, which may be associated with chemoreception, chemotaxis, and olfaction. Identifying and characterizing new GPCRs may uncover hidden aspects of parasite biology useful towards the development of novel intervention strategies.