The crown-of-thorns starfish (COTS) is a gonochoric broadcast spawner that forms dense spawning aggregations in response to endogenous and exogenous signals during summer. Aggregating COTS in captivity secrete an exoproteome cocktail of putative pheromones into the surrounding seawater that can elicit aggregation behaviour in conspecifics. However, it is not yet known how these putative pheromones are expressed during the summer spawning season, or how gravid COTS sense and respond to them. By comparing tissue-specific transcriptomes from wild-caught male and female COTS sampled during the summer spawning season, we identified 37 putative pheromones present in the aggregation-inducing exoproteome that are differentially expressed between the ovaries and testes, suggesting potential roles as pheromones regulating aggregation and synchronized spawning. Moreover, we found that gravid females differentially upregulate a large number of G-protein-coupled receptors, neurotransmitters and hormones in olfactory tissues such as sensory tentacles, suggesting that females are priming themselves to rapidly respond to potential pheromones. Consequently, we provide a deeper understanding of COTS spawning biology and identify sex-specific traits that may facilitate the synchronized reproductive behaviour between conspecifics. Further studies into these sex-specific differences may contribute to the development of novel biocontrol strategies.