Sensory biology is a critical component of organismal fitness and selection on sensory traits can drive macroevolutionary processes like speciation. Among mollusks, chemosensation (the detection of chemical signals) is an important sensory modality. The functional basis of chemosensation is a suite of olfactory receptor (OR) genes, but despite their importance to molluscan life history, ecology, and evolution, these genes remain poorly characterized for this highly diverse phylum. Here, we explore molluscan biology through this novel lens, using transcriptomics to characterize the olfactory receptor (OR) gene repertoires of Conus ebraeus Linnaeus, 1758 and C. judaeus Bergh, 1895—a pair of closely related, co-occurring gastropod species that exhibit fine-scale niche partitioning. We identify candidate OR genes, construct a gene tree for this gene family, and compare its structure and composition between these two species. We measure and compare gene expression of candidate OR genes, test for differential expression of orthologous loci, and compare patterns of sequence evolution between paralogous and orthologous loci to determine if gene family diversification occurs within or between species. Finally, we compare rates of evolution between ortholog pairs to identify genes showing evidence of differential selective pressures. Although C. ebraeus and C. judaeus share similar OR gene family repertoires, some genes showed divergence in terms of patterns of expression and modes of selection, which suggests the adaptive evolution of olfactory abilities among species. This is the first study to characterize the genetic basis of olfaction in Conus Linnaeus, 1758 and provides a genetic foundation for understanding how sensory biology can contribute to the rapid diversification of this genus.