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Abstract The establishment of reproductive isolation between species via gametic incompatibility initially requires within-species variation in reproductive compatibility. We investigate how within-species variation in sperm and egg recognition proteins, potentially generated via sexual conflict, influences reproductive isolation between two partially sympatric sea urchin species; the North American west coast Mesocentrotus franciscanus and the circumpolar Strongylocentrotus droebachiensis. Barriers to hybridization are stronger when eggs are given a choice of conspecific versus heterospecific sperm and the variation in hybridization among crosses can be explained by whether the sperm or egg protein variant is ancestral or derived. Derived proteins can be recognized as different and prevent hybridization. Examination of the allele frequencies of these proteins in M. franciscanus in and out of sympatry with S. droebachiensis along the west coast of North America reveals evidence of reinforcement selection and reproductive character displacement in eggs but not sperm, which likely reflects the differential cost of hybridization for males and females.