Coevolution of pairs of gamete recognition genes expressed on sperm and eggs can account for variation in reproductive compatibility between mates and the evolution of reproductive differences among populations. We fit branch-sites codon models to 1000 Genomes data to identify candidate sites under positive selection for high rates of amino acid substitution in the human egg coat genes ZP2 and ZP3, and in the sperm ZP receptor gene C4BPA. Six lines of evidence indicated that these candidate sites are coevolving under selection at fertilization. (1) The candidate site in each ZP gene occurred in the known sperm-binding domains. (2) The candidate site in C4BPA was the same coding sequence SNP identified as coevolving with ZP3 in a previous study using different methods and data. (3) All candidate sites distinguished two common haplotypes, with unusually high minor-allele frequencies. (4) Two candidate sites (in ZP2 and C4BPA) were correlated with variation in family size and birth interval lengths among Hutterite couples, and (5) were in linkage disequilibrium in the same Hutterite study population. (6) The same polymorphisms at these candidate sites are known from Neanderthal or Denisovan genomes (consistent with long-term balancing selection). This evidence supports a previously proposed hypothesis of selection on coevolving combinations of egg- and sperm-expressed alleles (in ZP3 and C4BPA), and point toward specific genetic variants that are the targets of selection, explain the coevolution of these three genes due to their epistatic interactions, underlie natural reproductive variation, and could be associated with clinical infertility.