Evolution of genetic (co)variances (the G-matrix) fundamentally influences multitrait divergence. Here, we isolated the contribution of two chromosomal quantitative trait loci (QTLs), a meiotic drive locus and a polymorphic inversion, to the overall G-matrix for a suite of floral, phenological and male fitness traits in a population of Mimulus guttatus. This allowed us to predict the evolution of trait means and genetic (co)variances as a function of allele frequencies, and to evaluate theories about the maintenance of genetic variation in fitness. Individuals generated using a replicated F(2) breeding design were grown under common conditions, genotyped and measured for trait values. Significant additive genetic variance existed for all traits, and most genetic covariances were significantly nonzero. Both QTLs contribute to the additive genetic (co)variances of multiple traits. Pleiotropy was not generally consistent, either between QTLs or with the genetic background. Shifts in allele frequencies at either QTL are predicted to result in substantial changes in the G-matrix. Both QTLs contribute substantially to the genetic variation in pollen viability. The Drive QTL, and perhaps also the inversion, demonstrates the contribution of balancing selection to the maintenance of genetic variation in fitness.