The study of sexual selection and reproductive biology are dynamic research fields that contribute to basic research, public health, agriculture, and conservation. Peromyscus mice are an important model for studying the evolution of reproductive traits shaped by sexual selection due to the natural diversity of mating systems in this genus. Like most rodents, the ancestral mating strategy of Peromyscus is believed to be promiscuity, but monogamy has evolved independently at least twice. In this dissertation, I investigate how the divergent mating systems in Peromyscus have shaped the diversity of reproductive traits using six species (three monogamous and three promiscuous). First, I characterize the estrous cycle and show that promiscuous species display more intense estrous signaling than monogamous species, but I find a uniform cycle length across the genus. Moreover, I report a method to hormonally-induce ovulation in two species, P. polionotus (monogamous) and P. maniculatus (promiscuous). Second, to investigate the co-evolution of male and female reproductive traits, I examined six species that have evolved under divergent sexual selection pressures and found a correlated expression of traits associated with sperm competition in males and control of fertilization in females. Third, I focus again on P. polionotus and P. maniculatus to examine how mating system influences male response to perceived competition for reproductive success using resident-intruder introductions. I found that while the males of monogamous species were highly aggressive toward rivals, the promiscuous species increased sperm production, which is predicted to increase fertilization success when females mate multiply. Together, this research both characterizes and functionally tests how evolutionary history and social interactions have shaped the diversity in reproductive traits of Peromyscus mice.