The seed-bearing capsule of sesame shatters at harvest. This wildish trait makes the crop unsuitable for mechanized harvesting and also restricts its commercial potential by limiting the cultivation for countries that have no access to low-cost labor. Therefore, the underlying genetic basis of the capsule shattering trait is highly important in order to develop mechanization-ready varieties for sustainable sesame farming. In the present study, we generated a sesame F2 population derived from a cross between a capsule shattering cultivar (Muganli-57) and a non-shattering mutant (PI 599446), which was used to construct a genetic map based on double-digest restriction-site-associated DNA sequencing. The resulting high-density genetic map contained 782 single-nucleotide polymorphisms (SNPs) and spanned a length of 697.3 cM, with an average marker interval of 0.89 cM. Based on the reference genome, the capsule shattering trait was mapped onto SNP marker S8_5062843 (78.9 cM) near the distal end of LG8 (chromosome 8). In order to reveal genes potentially controlling the shattering trait, the marker region (S8_5062843) was examined, and a candidate gene including six CDSs was identified. Annotation showed that the gene encodes a protein with 440 amino acids, sharing ∼99% homology with transcription repressor KAN1. Compared with the capsule shattering allele, the SNP change and altered splicing in the flanking region of S8_5062843 caused a frameshift mutation in the mRNA, resulting in the loss of function of this gene in the mutant parent and thus in non-shattering capsules and leaf curling. With the use of genomic data, InDel and CAPS markers were developed to differentiate shattering and non-shattering capsule genotypes in marker-assisted selection studies. The obtained results in the study can be beneficial in breeding programs to improve the shattering trait and enhance sesame productivity.