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Keel bone fractures (KBF) in laying hens are a major welfare problem in the egg production industry. While housing design and nutrition are known contributing factors, the role of genetics in KBF susceptibility is not well understood. The objective of this study was to estimate the heritability of KBF susceptibility and identify associated genomic regions and candidate genes in commercial laying hens. We used KBF assessment scores derived from radiographs of 1,060 white-feathered two-way crossbred hens housed in a quasi-commercial aviary system. A log-transformation was applied to the KBF scores to normalize the data. All hens were genotyped with a 60 K SNP chip. We fit a linear mixed model with a genomic relationship matrix to estimate variance components and heritability, and conducted a genome-wide association study to identify SNPs associated with KBF. Our results showed that KBF was low to moderately heritable, with an estimated heritability of 0.08 on the original trait scale, and 0.22 on the log-transformed scale. We identified four significant or suggestive haplotype blocks on chromosomes 2 and 20 that together explained 13.2 % of the total additive genetic variance. These blocks contain several candidate genes (including BCAS1, CYP24A1, PFND4, TSHZ2, and GDF6) that have been linked to calcium and vitamin D homeostasis, skeletal development, and bone density in humans and mice. These findings support the possibility that susceptibility to KBF is determined not only by genes influencing bone strength directly, but also by genes affecting the vitamin D metabolic pathway that regulates calcium reabsorption. Finally, one of the genomic regions on chromosome 20 was in close proximity to QTL that have previously been associated with egg production levels and age at sexual maturity in chickens. Overall, our findings contribute to our understanding of the genetic architecture of KBF susceptibility, its possible relationship to early egg production, and the physiological pathways that influence skeletal health in laying hens.