Understanding the architecture of genetic variation, that is the number, effect, location, and interaction, of genes responsible for phenotypic variability in nature is important for the understanding of microevolutionary processes. In this study, we have used a quantitative trait loci (QTL) approach to uncover the genetic architecture of fitness-relevant traits associated with reproduction and immune defense in male Bombus terrestris bumblebees. Three male reproductive investment traits, the number and length of the produced sperm and the size of the accessory glands, were studied. Two branches of the insect innate immune system, the activation of the Phenoloxidase-cascade and the hemolymph's antibacterial activity, were investigated. We found that variation in most of the studied traits is based on a network of minor QTLs and epistatic interactions. Unexpectedly, there was no evidence for phenotypic or genetic trade-offs between the presumably costly investment in immune defense and reproductive effort in this population for the measured traits. In fact, we found a positive correlation, both, in phenotype and genetic architecture for the number of produced sperm and antibacterial activity against an insect pathogen. A major finding for all traits analyzed was that the epistatic interactions accounted for a major proportion of the explained phenotypic variance. Especially for traits involved in immune defense, this pattern highlights the possible role of parasites in the evolution and maintenance of recombination and sexual reproduction.