The haplodiploid wasp genus Nasonia is a promising model for studying the evolution of genic incompatibilities due to the existence of interfertile species and haploid males. The latter allows for significantly reducing the sample size required to detect and map recessive dysfunctional genic interactions. We exploited these features to study the genetics of intrinsic hybrid inviability in male F2 hybrids of Nasonia giraulti and N. vitripennis. Analyzing marker segregation in 225 hybrid embryos, we inferred a linkage map with 38 framework markers. The markers were tested for marker transmission ratio distortion (MTRD) and interchromosomal linkage disequilibrium in populations of embryonic and adult hybrids. We found evidence for four transmission ratio distorting loci (TRDL). Three TRDL showed a deficit of the N. giraulti allele in hybrids with N. vitripennis cytoplasm. A separate TRDL exhibited a deficiency of the N. vitripennis allele in hybrids with N. giraulti cytoplasm. We ascribe the observed MTRD in adult hybrids to cytonuclear genic incompatibilities causing differential mortality during development since hybrid embryos did not show MTRD. The identified cytonuclear genic incompatibilities in F2 hybrids with N. vitripennis cytoplasm account for most of the intrinsic hybrid inviability in this cross. The high mortality rate in F2 hybrids with N. giraulti cytoplasm cannot be explained by the single identified TRDL alone, however.