The potential effect of population outbreaks on within and between genetic variation of populations in pest species has rarely been assessed. In this study, we compare patterns of genetic variation in different sets of historically frequently outbreaking and rarely outbreaking populations of an agricultural pest of major importance, the migratory locust, Locusta migratoria. We analyse genetic variation within and between 24 populations at 14 microsatellites in Western Europe, where only ancient and low-intensity outbreaks have been reported (non-outbreaking populations), and in Madagascar and Northern China, where frequent and intense outbreak events have been recorded over the last century (outbreaking populations). Our comparative survey shows that (i) the long-term effective population size is similar in outbreaking and non-outbreaking populations, as evidenced by similar estimates of genetic diversity, and (ii) gene flow is substantially larger among outbreaking populations than among non-outbreaking populations, as evidenced by a fourfold to 30-fold difference in FST values. We discuss the implications for population dynamics and the consequences for management strategies of the observed patterns of genetic variation in L. migratoria populations with contrasting historical outbreak frequency and extent.