The Latvian Darkheaded is the only locally developed sheep breed. The breed was formed at the beginning of the 20th century by crossing local coarse-wooled sheep with the British Shropshire and Oxfordshire breeds. The breed was later improved by adding Ile-de-France, Texel, German blackheads, and Finnsheep to achieve higher prolificacy and better meat quality. Previous studies have reported the Latvian Darkheaded sheep to be closely related to Estonian and Lithuanian Blackface breeds, according to microsatellite data. To expand our knowledge of the genetic resources of the Latvian Darkheaded breed, we conducted a whole-genome resequencing analysis on 40 native sheep. The investigation showed that local sheep harbor genetic diversity levels similar to those observed among other improved breeds of European origin, including Charollais and Suffolk. Genome-wide nucleotide diversity (π) in Latvian Darkheaded sheep was 3.91 × 10, whereas the average observed heterozygosity among the 40 animals was 0.267 and 0.438 within the subsample of unrelated individuals. The has rapidly decreased to 200 ten generations ago with a recent drop to 73 four generations ago. However, inbreeding levels based on runs of homozygosity were, on average, low, with F ranging between 0.016 and 0.059. The analysis of the genomic composition of the breed confirmed shared ancestry with sheep of British origin, reflecting the history of the breed. Nevertheless, Latvian Darkheaded sheep were genetically separable. The contemporary Latvian Darkheaded sheep population is genetically diverse with a low inbreeding rate. However, further development of breed management programs is necessary to prevent an increase in inbreeding, loss of genetic diversity, and depletion of breed-specific genetic resources, ensuring the preservation of the native Latvian Darkheaded sheep.