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Sheep production contributes to a secure and diverse food and fibre supply in the United States, with growing ethnic diversity strengthening demand. Katahdin is a composite hair-type sheep breed developed in the United States that has become the most popular breed in many regions of the country and the first one to have genomic selection implemented in its breeding program. Therefore, the main objectives of this study were to estimate variance components of reproductive traits, including number of lambs born (NLB), number of lambs weaned (NLW), age at first lambing (AFL), and interval from first to second lambing (LI), in Katahdin sheep using the AIREML method and the single-step Genomic Best Linear Unbiased Prediction (ssGBLUP) approach, and to identify genomic regions and candidate genes associated with these traits. The datasets used consisted of 127,536 animals in the pedigree, phenotypic records of 56,128 parities from 24,067 ewes, and genomic data from 10,032 animals with 30,308 single-nucleotide polymorphisms (SNP) after quality control. Analyses were performed using the BLUPF90 family of programs. We observed low heritability estimates for all studied traits (0.09 ± 0.00 for NLB, 0.08 ± 0.00 for NLW, 0.09 ± 0.01 for AFL, and 0.08 ± 0.01 for LI). The genetic correlations between the traits ranged from 0.17 ± 0.02 (AFL and LI) to 0.79 ± 0.02 (NLB and NLW). All traits were found to be highly polygenic with all 14 significant SNP on eight (OAR) chromosomes (3, 6, 7, 8, 9, 12, 13, and 15) having small effects on the total variability on the traits. These SNP were located near or within 18 candidate genes: four genes associated with NLB (AAK1, GFPT1, SLC23A2, and GDAP1), four with NLW (ARHGAP18, TTLL2, UNC93A, and GPR31), six with AFL (NAP1L5, FAM13A, HS3ST1, CCDC181, NME7, and BLZF1), and four with LI (TAF4, CDH4, CADM1, and SEL1L). These candidate genes have been previously associated with fertility, embryonic development, growth, disease resistance, and climatic adaptation traits. Our findings indicate that fertility and reproduction traits in Katahdin sheep can be improved through direct genetic selection. Genetic improvement for these traits will benefit from genomic selection as more accurate estimates of breeding values for selection candidates can be obtained at a younger age. Although the studied traits are influenced by a complex interplay of genetic and environmental factors, the candidate genes identified enabled a better understanding of the biological mechanisms underlying reproductive performance in Katahdin sheep.