Progeny from full-sib/half-sib families of a population of Callosobruchus maculatus near genetic equilibrium were reared either in an ancestral (30°C, 70 per cent relative humidity) or in a novel (25°C, 45 per cent relative humidity) environment. The life history traits, emergence body weight and development period were measured in both sexes. Insects developed faster and emerged heavier at a higher temperature and humidity. For both sexes, in the ancestral environment additive genetic variation and 'narrow-sense' heritability estimates were higher for body weight, the morphological trait, than for development period, the primary fitness trait. For both sexes, matrix analyses revealed significant differences between the estimated additive genetic variance-covariance (G) matrices from each environment. In the novel environment, the evolved genetic architecture appeared to break down, possibly as a result of novel gene expression; the trade-off between emergence body weight and development period was disrupted with an associated increase in additive genetic variation for both life history traits. In both environments, female insects developed more slowly and emerged heavier than male insects. Matrix analyses show significant differences between the G-matrices of each sex, suggesting that different constraints may operate in the two sexes.