Genetic effects and radioactive contamination of large mammals, including wild boar (Sus scrofa), have been studied in Japan because of dispersal of radionuclides from the Fukushima Dai-ichi Nuclear Power Plant in 2011. Such studies have generally demonstrated a declining trend in measured radiocesium body burdens in wildlife. Estimating radiation exposure to wildlife is important to understand possible long-term impacts. Here, radiation exposure was evaluated in 307 wild boar inhabiting radioactively contaminated areas (50–8000 kBq m⁻²) in Fukushima Prefecture from 2016 to 2019, and genetic markers were examined to assess possible germline mutations caused by chronic radiation exposures to several generations of wild boar. Internal Cs activity concentrations in boar remained high in areas near the power plant with the highest concentration of 54 kBq kg⁻¹ measured in 2019. Total dose rates to wild boar ranged from 0.02 to 36 μGy h⁻¹, which was primarily attributed to external radiation exposure, and dose rates to the maximally exposed animals were above the generic no-effects benchmark of 10 μGy h⁻¹. Using the estimated age of each animal, lifetime radiation doses ranged from <0.1 mGy to 700 mGy. Despite chronic exposures, the genetic analyses showed no significant accumulation of mutation events. Because wild boar is an occasional human dietary item in Japan, effective dose to humans from ingesting contaminated wild boar meat was calculated. Hypothetical consumption of contaminated wild boar meat from radioactively contaminated areas in Fukushima, at the per capita pork consumption rate (12.9 kg y⁻¹), would result in an average effective annual dose of 0.9 mSv y⁻¹, which is below the annual ingestion limit of 1 mSv y⁻¹. Additionally, a consumption rate of about 1.4 kg y⁻¹ of the most contaminated meat in this study would not exceed annual ingestion limits.