The ultimate causes of honest signaling remain a subject of debate, with questions remaining over the relative importance of costs and constraints. Signal costs may make dishonesty prohibitively expensive, while genetic constraints could make it impossible. We investigated honest signaling using full-sib analysis and parent-offspring regression in the ant Lasius niger, in which queens produce a cuticular hydrocarbon-based pheromone that signals fertility and inhibits worker reproduction and aggression. We found multiple lines of evidence that cuticular hydrocarbon production is genetically correlated with oogenesis and that the queen pheromone 3-methylhentriacontane and other 3-methylalkanes have strong genetic links with fertility relative to other cuticular hydrocarbons. These genetic correlations may maintain honesty in the face of directional selection on signaling and explain the putatively widespread use of cuticular hydrocarbons in fertility signaling across the social insects. We also found evidence for a positive genetic correlation for fertility between the castes; that is, the most fertile queens produced especially fertile workers. These results highlight that intercaste genetic correlations could constrain the evolution of queen-worker dimorphism, such that worker reproduction may sometimes reflect a nonadaptive ‘caste load’ rather than positively selected cheating.