Many agricultural pest species occur in seasonal metapopulations with a period of asexual reproduction. We use evolutionary theory to predict timing of dispersal for such species, and identify four sequential phases: no dispersal, dispersal from initially occupied patches, dispersal from later colonized patches, and no dispersal. The third type of phase occurs only when reproductive rates are relatively high; we speculate that this could explain why among aphids there can be either one or two waves of dispersal during a season, depending on the species. Our model also explains other features of aphid biology, including a summer crash in colony size, and a decline in the number of colonies towards the end of each reproductive season. The presence of an additional surge of dispersal becomes more likely as season length increases, and does not require further evolution. This could have profound implications for pest management during future climatic warming.