We estimated broad-sense heritabilities (H(2)) of 13 female and seven male life-history traits of the Glanville fritillary butterfly (Melitaea cinxia) under semi-natural conditions in a large outdoor population cage. The analysis was based on full-sib families collected as young larvae in the field and reared under common garden conditions. We found significant genetic variance in female lifespan, fecundity, number of matings and host-plant preference as well as in male body mass and mobility. Apart from host-plant preference, female traits that were more strongly correlated with lifetime reproductive success (LRS; measured as total number of eggs laid) had higher H(2). LRS itself exhibited significant heritability. Host-plant preference had very high H(2), consistent with a previously reported genetically determined geographical cline in host-plant preference in the study area. Lifespan and egg hatching rate were significantly associated with a SNP in the coding region of the Pgi gene, for which there is previous evidence for balancing selection. Selection on Pgi, which furthermore shows spatial and temporal variation, may maintain genetic variance in fitness-related life-history traits. In contrast, we found no strong evidence for life-history trade-offs.