The desert locust (Schistocerca gregaria) undergoes crowding-induced phase transformation from solitary form to gregarious form. The transformations involves changes in behaviour, colour, development, morphometry, fecundity and endocrine physiology. Recession populations of the desert locust exist primarily in the solitary phase as small populations in patchy environments and are prone to extinction because of climatic events. Significant genetic differentiation among recession populations along the Red Sea coast of Eritrea was previously reported. It was hypothesized that despite the mixing effect of recurrent swarms, metapopulation dynamics could have produced genetic divergence among these highly scattered recession populations. A Monte Carlo simulation of the population dynamics of the desert locust in a metapopulation setting, with a realistic range of parameter values clearly demonstrated that this is possible. Population growth was represented by a discrete-time logistic equation. The duration of recessions and swarms was sampled from normal distributions whose means and standard deviations were varied based on reported estimates. An average recession duration of 10 ± 3 generations and swarm periods half as long but almost twice as variable produced a partitioning of the total genetic variance most similar to that in the empirical study. In conventional metapopulation analysis, whether turnover leads to increased or reduced divergence is dependent on the number of colonists relative to the number of recurrent migrants, and on whether the colonists arise from a single patch or many patches. In the case of locusts, the stochastic boom and bust cycle is the overriding factor. Divergence between patches during recession due to founder effect and recurrent drift is balanced by the high rate of mixing during plagues.