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We analyzed variations in 90 mitochondrial DNA (mtDNA) D-loop and heat shock protein 70 (HSP70) gene sequences from four populations of domesticated helmeted Guinea fowls (70 individuals) and 1 population of wild helmeted Guinea fowls (20 individuals) in Kenya in order to get information about their origin, genetic diversity, and traits associated with heat stress. 90 sequences were assigned to 25 distinct mtDNA and 4 HSP70 haplotypes. Most mtDNA haplotypes of the domesticated helmeted Guinea fowls were grouped into two main haplogroups, HgA and HgB. The wild population grouped into distinct mtDNA haplogroups. Two mtDNA haplotypes dominated across all populations of domesticated helmeted Guinea fowls: Hap2 and Hap4, while the dominant HSP70 haplotype found in all populations was CGC. Higher haplotype diversities were generally observed. The HSP70 haplotype diversities were low across all populations. The nucleotide diversity values for both mtDNA and HSP70 were generally low. Most mtDNA genetic variations occurred among populations for the three hierarchical categories considered while most variations in the HSP70 gene occurred among individuals within population. The lack of population structure among the domestic populations could suggest intensive genetic intermixing. The differentiation of the wild population may be due to a clearly distinct demographic history that shaped its genetic profile. Analysis of the Kenyan Guinea fowl population structure and history based on mtDNA D-loop variations and HSP70 gene functional polymorphisms complimented by archaeological and linguistic insight supports the hypothesis that most domesticated helmeted Guinea fowls in Kenya are related to the West African domesticated helmeted Guinea fowls. We recommend more molecular studies on this emerging poultry species with potential for poverty alleviation and food security against a backdrop of climate change in Africa.