Chicken production, both in the local and commercial sectors, contributes significantly to human livelihood and food security. Precise use of diverse genetic resources is primary in breeding programs. The study analyzed the genetic diversity and population structure of commercial chickens and indigenous chicken ecotypes from three different agro-ecological zones (Semi-Deciduous Rainforest Zone, Guinea Savannah, and Coastal Savannah) using SilicoDArT and SNP markers, utilizing whole-genome sequencing and phenotypic data. Phenotypic data were collected from 72 indigenous chicken ecotypes across the three AEZs, and 32 commercial birds kept at the Kwame Nkrumah University of Science and Technology (KNUST). DNA samples used for sequencing were obtained from 88 chickens (62 indigenous chicken ecotypes and 26 commercial chickens). A total of 54,995 SilicoDArT and 85,396 SNPs markers were generated from DArTseq genotyping. After filtering, 44,784 SilicoDArT and 58,353 SNP were used for genetic diversity and population structure analysis. Both markers showed high reproducibility and call rate. Polymorphic information content (PIC) values ranged from 0.00 to 0.50, while ≥ 50 % showed PIC values more than the median. Furthermore, we obtained FST values, Nei’s genetic distance, dendrogram analysis, and principal component analysis (PCA) of commercial and indigenous chickens. The FST and Nei’s genetic distance showed that there is high genetic diversity between the commercial chickens and the indigenous chicken ecotypes. However, there was low genetic diversity among the indigenous chicken ecotypes. The PCA analysis indicated a clear separation between the commercial and indigenous chicken ecotypes, while no clear separation was observed between the indigenous chicken ecotypes. The phenotypic data and the dendrogram indicated that naked and frizzle genes do not markedly alter the genetics of indigenous and commercial birds, and their influence on economic traits may be solely determined by the prevailing environmental conditions. The results indicate that there is high genetic differentiation between commercial and indigenous chickens based on SilicoDArT and SNP markers. The indigenous chickens from the agro-ecological zones have low genetic diversity and might have a common origin. Naked neck and frizzle genes do not markedly alter the genetic performance of birds in terms of economic traits. Therefore, the superiority of birds carrying these genes in economic traits may be solely due to environmental variation.