<p>Without a high-quality whole genome sequence, it is impossible to determine the extent to which the markers in a high-resolution linkage map cover the total length of chromosomes. To evaluate the coverage of a high-resolution linkage map of onion (<i>Allium cepa</i> L.), the positions of 651 markers on the linkage map were identified within the onion whole genome sequence. The linkage and physical maps showed a high degree of collinearity. Nevertheless, large regions at the distal ends of some chromosomes lacked marker coverage. To improve this, 33 additional markers were developed based on their physical locations. The length of the improved linkage map increased from 749.8 to 808.5&#xa0;cM. Using this improved map, the frequency and distribution of crossovers (COs) were analyzed. The average number of COs per chromatid was estimated at 0.95. This is the first estimation of CO frequency in onion using a high-resolution linkage map. CO rates (cM/Mb) were generally high at distal regions of chromosomes, but were completely suppressed at the putative centromeres. Notably, COs were strongly suppressed on the short arm of chromosome 8. Among the 684 markers comprising the linkage map, 104 markers were analyzed to estimate polymorphism information content (PIC) values of markers using 48 onion cultivars, and pairwise genetic distances among cultivars were calculated. Interestingly, the PCoA plot revealed clear clustering of cultivars based on their maturity. Considering PIC values and positions of markers, eight markers showing high PIC values were chosen as an optimal marker set for onion cultivar identification, along with three markers for cytoplasm identification and <i>Ms</i> genotyping.</p>