Exposure to seminal fluid has been shown to benefit female fertility by inducing immune responses within the female tract that aid in implantation and placental development. Recent epidemiological studies have looked into partner-specific effects of seminal fluid exposure, as the fluid contains major histocompatibility complexes (MHCs) that are unique to each individual and are able to interact with the maternal immune system. We tested the hypothesis that extended exposure to a male’s seminal fluid of a specific genetic background and MHC haplotype will benefit future pregnancies sired by the same genotype of male due to the fetus presenting the same MHC. This has been predicted from human studies where having multiple pregnancies with one partner shows a decreasing risk of adverse outcomes with each subsequent pregnancy while switching to a new partner for later pregnancies returns the risk to the initial level. Using mice, we initially housed females with other females or with one of two genotypes of vasectomized males that only produce seminal fluid and are of differing MHCs/strains to each other; females were then mated to intact males of either the same or different MHC/strain than they had experienced previously to assess their subsequent fertility. We found a decrease in the number of reabsorptions in females previously exposed to the same MHC/strain males earlier in life and an increase in maternal weight, fat and lean body composition during gestation. We also observed a negative effect of prior exposure to males of a different MHC/strain relative to controls, with females experiencing greater pup death and restricted pup growth during lactation. Prior research has established the importance of seminal fluid in supporting healthy pregnancies; however, our findings suggest that these effects may vary depending on the partners encountered during different stages of sexual history.