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Background Despite the broad distribution of leishmaniasis in Iran, there is a little genetic information about the causative agents and epidemiological status of the disease. Genetic diversity of the parasite is suggested to be one of the factors, which influences the clinical manifestations of the disease. In this study, we investigated the genetic variations, population structure, and evolutionary history of Leishmania species from endemic foci of Iran. Methods Fifty-two isolates from humans, canines, and rodents from different endemic foci of Iran were used to sequence the N-acetyl glucosamine-1-phosphate transferase (Nagt) gene. Phylogenetic and structure analyses were performed to investigate inter-and intra-species diversity of the Leishmania isolates. Results In total, 10 haplotypes including L. major (n = 6), L. tropica (n = 2), L. infantum (n = 1) and L. turanica (n = 1) were identified across 52 isolates. Haplotype diversity (Hd) ranged from zero for L. infantum and L. turanica to 0.78 ± 0.136 for L. major. This study identified population structure of Leishmania isolates from different geographical regions of Iran. The results of the phylogenetic tree showed 4 distinct clades for each species of Leishmania. In addition, the highest intraspecies diversity was observed among L. major isolates. No correlation was observed between species and geographic distribution of haplotypes. Conclusions Leishmania isolates were identified at the species level using the Nagt gene, low variation within species indicates conservation of this gene in Leishmania. The results provide knowledge into the evolutionary history of Iranian Leishmania isolates.