SummaryReproduction in wild animals can divert limited resources away from immune defence, resulting in increased parasite burdens. A longstanding prediction of life history theory states that these parasites can harm the reproductive individual, reducing its subsequent fitness and producing reproduction-fitness tradeoffs. Here, we examined associations among reproductive allocation, immunity, parasitism, and subsequent fitness in a wild population of individually identified red deer (Cervus elaphus). Using path analysis, we investigated whether costs of lactation for downstream survival and fecundity were mediated by changes in strongyle nematode count and mucosal antibody levels. Lactating females exhibited increased parasite counts, which were in turn associated with substantially decreased fitness in the following year in terms of overwinter survival, fecundity, subsequent calf weight, and parturition date. This study offers observational evidence for parasite regulation of multiple life history tradeoffs, supporting the role of parasites as an important mediating factor in wild mammal populations.