Local Sudanese sheep populations inhabiting diverse environmental conditions and holding opposing morphologies provide opportunities for molecular-genetic research. Characterizing their genome is crucial for sustainable breeding improvement and targeting favorable genes in breeding programs. However, the genome of these sheep populations, which comprises several subtypes, remains uncharacterized using whole-genome sequence data. This study aimed to elucidate genome-wide genetic diversity and population structure of 11 local Sudanese sheep populations, namely, Hammari, Kabbashi, Meidobe, Ashgar, Dubasi, Watish, Bega, Naili, Fulani, Zagawi, and Garag. Ninety whole blood samples were collected, and we extracted DNA using a Qiagen DNeasy® extraction kit. We used the Illumina HiSeq 2000 platform to sequence all the DNA samples. We included whole-genome sequence data of three Ethiopian sheep (Doyogena, Kefis, and Gafera) and one Libyan sheep (Libyan Barbary) in the study to infer the genetic relationships of local Sudanese sheep populations from a continental perspective. A total of 44.8 million bi-allelic autosomal SNPs were detected; 28.5% and 63.3% occur in introns and intergenic regions, respectively. The mean genetic diversity ranged from 0.276 for Garag to 0.324 for Kabbashi sheep populations. The lowest FST estimates were observed between Kabbashi and Ashgar and the highest between Bega and Fulani local Sudanese sheep populations. The principal component and population structure analyses of the 11 local Sudanese sheep populations indicated three separate genetic groups categorized following their tail morphotype, geographical distribution, and population subtype. The thin-tailed local Sudanese sheep populations exhibited independent clustering from the fat-tailed Ethiopian and Libyan sheep. We also observed distinct clustering between the fat-tailed Ethiopian and Libyan sheep. The present study’s findings demonstrated the population structure and principal components related to tail morphotype, geographical distribution, and population subtype of local Sudanese sheep populations. A clear signature of admixture was observed among the studied local Sudanese sheep populations.