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Zoonotic cutaneous leishmaniasis (ZCL) caused by <i>Leishmania major</i> Yakimoff & Shokhor and transmitted by <i>Phlebotomus papatasi</i> (Scopoli) is a public health concern in Morocco. The disease is endemic mainly in pre-Saharan regions on the southern slope of the High Atlas Mountains. The northern slope of the High Atlas Mountains and the arid plains of central Morocco remain non-endemic and are currently considered high risk for ZCL. Here we investigate and compare the population genetic structure of <i>P. papatasi</i> populations sampled in various habitats in historical foci and non-endemic ZCL areas. A fragment of the mtDNA <i>cytochrome oxidase I (COI)</i> gene was amplified and sequenced in 59 individuals from 10 <i>P. papatasi</i> populations. Haplotype diversity was probed, a median-joining network was generated (<i>F</i>_ST) and molecular variance (AMOVA) were analyzed. Overall, we identified 28 haplotypes with 32 distinct segregating sites, of which seven are parsimony informative. The rate of private haplotypes was high; 20 haplotypes (71.4%) are private ones and exclusive to a single population. The phylogenetic tree and the network reconstructed highlight a genetic structuration of these populations in two well defined groups: Ouarzazate (or endemic areas) and Non-Ouarzazate (or nonendemic areas). These groups are separated by the High Atlas Mountains. Overall, our study highlights differences in terms of population genetics between ZCL endemic and non-endemic areas. To what extent such differences would impact the transmission of <i>L. major</i> by natural <i>P. papatasi</i> population remains to be investigated.