The dopaminergic signaling pathway is involved in many physiological functions in vertebrates, but poorly documented in protostome species except arthropods. We functionally characterized a novel dopamine receptor in the Pacific oyster (Crassostrea gigas), activated by dopamine and tyramine with different efficacy and potency orders. This receptor — Cragi-DOP2R — belongs to the D1-like family of receptors and corresponds to the first representative of the Dop2/invertebrate-type dopamine receptor (Dop2/INDR) group ever identified in Lophotrochozoa. Cragi-DOP2R transcripts were expressed in various adult tissues, with higher expression levels in the visceral ganglia and the gills. Following an experiment under acute osmotic conditions, Cragi-DOP2R transcripts significantly increased in the visceral ganglia and decreased in the gills, suggesting a role of dopamine signaling in the mediation of osmotic stress. Furthermore, a role of the Cragi-DOP2R signaling pathway in female gametogenesis and in early oyster development was strongly suggested by the significantly higher levels of receptor transcripts in mature female gonads and in the early embryonic stages.