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Colonizing populations at the leading edge of range expansion are expected to have a reduced genetic diversity and strong genetic structure caused by genetic drift and allele surfing. Until now, few studies have found the genetic signatures of allele surfing in expanding wild populations. Using mtDNA markers, we studied the genetic structure of the population of midday gerbils (Meriones meridianus) expanding their range to the west in Kalmykia (southern Russia) following the new cycle of desertification, re-colonizing areas abandoned in the mid-2010s. In the colonizing population, we found a reduced genetic diversity, the redistribution of haplotype frequencies—in particular, in favor of variants rare in the core population—and strong genetic structure combined with strong differentiation from the core population—patterns suggestive of allele surfing on the wave of expansion. In terms of genetic diversity and spatial structuration, the western edge population sampled in 2008 before its collapse in 2017 occupies the intermediate position between the current colonizing and core population. This suggests that reduced genetic diversity and increased genetic differentiation are general features of marginal populations, enhanced by the founder and allele-surfing effects at the leading edges of expanding ranges.