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We investigated the genetic diversity and population genetic structure of six morphologically distinct Ethiopian donkey populations using 12 equine microsatellite markers. The donkey populations were Abyssinian (AB), Afar (AF), Hararghe (HA), Ogaden (OG), Omo (OM) and Sinnar (SI). Blood samples were collected from 180 genetically unrelated donkeys (30 individuals per population). Population genetic diversity estimates showed that total number and mean number of observed alleles, average observed and expected heterozygosity were 94, 5.208 ± 0.0229, 0.555 ± 0.023 and 0.588 ± 0.022, respectively. Highly significant deficiency in heterozygote was detected within the overall samples (F IS = 0.055 ± 0.021; P < 0.001). Though highly significant (P < 0.001), heterozygote deficiency within populations relative to total population was moderate (F ST = 0.046 ± 0.016), suggesting a higher diversity within the populations (95.4%) than between populations. Various genetic distance estimation methods produced a similar topology of un-rooted dendrograms that grouped the overall Ethiopian donkeys into lowland (Ogaden, Omo and Sinnar) and highland (Abyssinian, Afar and Hararghe) genetic lineages. Likewise, Bayesian clustering analysis produced a similar pattern of clustering that was highly concordant with traditional donkey classification systems in Ethiopia.