We conducted an integrated, long-term field and genomic analysis of >20 local populations of Dolly Varden (Salvelinus curilus) over a 25-year period in the upper Sorachi River, Hokkaido, Japan. During this time, populations experienced substantial environmental changes, including climate warming, flood disturbances, and river channel modifications. These changes led to diverse impacts, such as local extinctions, declines in genetic diversity, shifts in spawning phenology, and altered migratory behavior. Despite these local-level changes, the overall metapopulation remained relatively stable in terms of demographic trends and genetic structure. Population size and connectivity were key factors, suggesting that dispersal among local populations plays a stabilizing role in both demography and genetic composition. These findings demonstrate how demographic dynamics and allele frequency changes—i.e., microevolution—interact in wild populations.