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ABSTRACT Shared polymorphisms, loci with identical alleles across species, are of unique interest in evolutionary biology as they may represent cases of selection maintaining ancient genetic variation post‐speciation, or contemporary selection promoting convergent evolution. In this study, we investigate the abundance of shared polymorphism between two members of theDaphnia pulexspecies complex. We test whether the presence of shared mutations is consistent with the action of balancing selection or alternative hypotheses such as hybridization, incomplete lineage sorting or convergent evolution. We analyzed over 2,000 genomes from six taxa in theD. pulexspecies group and examined the prevalence and distribution of shared alleles between the focal species pair, North American and EuropeanD. pulex. We show that North American and EuropeanD. pulexdiverged over 10 million years ago, yet retained tens of thousands of shared polymorphisms. We suggest that the number of shared polymorphisms between North American and EuropeanD. pulexcannot be fully explained by hybridization or incomplete lineage sorting alone. We show that most shared polymorphisms could be the product of convergent evolution, that a limited number appear to be old trans‐specific polymorphisms, and that balancing selection is affecting convergent and ancient mutations alike. Finally, we provide evidence that a blue wavelength opsin gene with trans‐specific polymorphisms has functional effects on behavior and fitness in the wild.