The matrix of genetic variances and covariances (G matrix) represents the genetic architecture of multiple traits sharing developmental and genetic processes and is central for predicting phenotypic evolution. These predictions require that the G matrix be stable. Yet the timescale and conditions promoting G matrix stability in natural populations remain unclear. We studied stability of the G matrix in a 20-year evolution field experiment, where a population of the cosmopolitan parthenogenetic soil nematode Acrobeloides nanus was subjected to drift and divergent selection (benign and stress environments). Selection regime did not influence the level of absolute genetic constraints: under both regimes, two genetic dimensions for three life-history traits were identified. A substantial response to selection in principal components structure and in general matrix pattern was indicated by three statistical methods. G structure was also influenced by drift, with higher divergence under benign conditions. These results show that the G matrix might evolve rapidly in natural populations. The observed high dynamics of G structure probably represents the general feature of asexual species and limits the predictive power of G in phenotypic evolution analyses.