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Beet necrotic yellow vein virus (BNYVV) is the causal agent of rhizomania, the most serious sugar beet disease worldwide. Since the first finding in Japan in 1969, BNYVV became widespread throughout Hokkaido in a few decades and led to the introduction of Rz1‐resistant sugar beet cultivars in the 1990s. Here, we report the historical progress of the BNYVV epidemic in Hokkaido from 1969 to 2019. Previous analysis on samples from 1991 showed that BNYVV isolates were classified into three strains (named O, D, and T) based on the RNA3‐encoded p25 gene. The O‐type viruses were widely detected in Hokkaido, while the D‐ and T‐type viruses were detected in limited areas. The RNA5, encoding the p26 gene, was initially contained in some D‐ and O‐type isolates but not in any T‐type isolates. Interestingly, recent sample analysis revealed that RNA5‐containing T‐type viruses, seemingly more virulent than the other two strains, were widely detected in Hokkaido. Additionally, a small group of virus isolates harbouring a new p25 gene (named C) was found in limited areas. These results suggest that the T‐type viruses, which accompanied RNA5, have been preferentially spread from a limited area to other districts over the last few decades and that this spread might be strongly associated with the recent introduction of Rz1‐resistant sugar beet cultivars. BNYVV‐positive samples also contained mainly beet soil‐borne virus and traces of beet virus Q, both of which are the first to be recorded in Japan. [ABSTRACT FROM AUTHOR]