Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signaling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric broadcast spawning coral Astrangia poculata. We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity is necessary for PKA activation, and PKA activity is also required for motility. Ultrastructures of A. poculata sperm displayed morphological homology with other gonochoric cnidarians, and investigation of cnidarian proteomes revealed that sAC exhibits broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-PKA signaling in sperm motility across coral sexual systems and suggest that the role of this pathway in sperm motility is likely ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification.