The persistence and dynamics of populations largely depends on the way they are configured and integrated into space and the ensuing eco-evolutionary dynamics. We manipulated spatial and temporal variation in patch size in replicated experimental metapopulations of the herbivore mite Tetranychus urticae. Evolution over approximately 30 generations in the spatially and spatiotemporally variable metapopulations induced a significant divergence in life history traits, physiological endpoints and gene expression, but also a remarkable convergence relative to the stable reference patchy metapopulation in traits related to size and fecundity and in its transcriptional regulation. The observed evolutionary dynamics are tightly linked to demographic changes, more specifically frequent episodes of resource shortage, and increased the reproductive performance of mites on tomato, a challenging host plant. This points towards a general, adaptive stress response in stable spatial variable and spatiotemporal variable metapopulations that pre-adapts a herbivore arthropod to novel environmental stressors.