<p>Virus yellows (VY) have emerged as a considerable threat to sugar beet production, particularly following the prohibition of neonicotinoid insecticides, which were previously essential for controlling aphid vectors responsible for transmitting VY. In Japan, the beet leaf yellowing virus (BLYV) is prevalent; however, its effects on yield and heritability remain unclear before this study. This study assessed BLYV tolerance and its effect on yield-related traits over four years using 31 genotypes, including breeding genotypes, genetic resources, and F1 hybrids. Seedlings were artificially inoculated with BLYV in a controlled environment and then transplanted to the field in a randomized and replicated design, while uninoculated seedlings served as controls; subsequent strict pest management prevented further infection. Leaf yellowing symptoms were evaluated using the yellowing index (YI), and the plants were classified into strong, medium, medium-weak, and weak tolerance groups. After accounting for year and other factors, YI was significantly correlated with root weight, Brix, and sugar yield (<i>p</i> &lt; 0.01), with stronger tolerance associated with lower sugar yield losses (overall mean 33.7%, range 5.5–64.0%). F1 tolerance to BLYV was correlated with parent tolerance, with a significant correlation between F1 and mid-parent YI (<i>rho</i> = 0.82–0.90, <i>p</i> &lt; 0.01), indicating heritability of BLYV tolerance (broad-sense heritability, <i>h</i>² = 0.45–0.50). This study provides two key insights: (1) selecting for reduced yellowing symptoms is an effective strategy for BLYV tolerance, confirmed after accounting for year effects and other minor diseases, and (2) breeding F1 tolerance can be predicted based on tolerant parents.</p>