Abstract Exposure to radiation is a natural part of our environment. Yet, due to nuclear accidents such as at Chernobyl, some organisms are exposed to significantly elevated dose rates. Our understanding of the effects of radiation in the environment is limited, confounded by substantial interspecific differences in radio‐sensitivity and conflicting findings. Here we study radiation impacts on bumblebees in the laboratory using principles from life‐history theory, which assume organismal investment in fitness‐related traits is constrained by resource availability and resource allocation decisions. To investigate how chronic radiation might negatively affect life‐history traits, we tested whether exposure affects bumblebee energy budgets by studying resource acquisition (feeding) and resource use (metabolic rate). We monitored metabolic rate, movement and nectar intake of bumblebees before, during and after 10 days of radiation exposure. Subsequently, we monitored feeding and body mass across a dose rate gradient to investigate the dose rate threshold for these effects. We studied dose rates up to 200 μGy/hr: a range found today in some areas of the Chernobyl Exclusion Zone. Chronic low‐dose radiation affected bumblebee energy budgets. At 200 μGy/hr nectar consumption elevated by 56% relative to controls, metabolic CO2 production increased by 18%, and time spent active rose by 30%. Once radiation exposure stopped, feeding remained elevated but CO2 production and activity returned to baseline. Our analysis indicates that elevated metabolic rate was not driven by increased activity but was instead closely associated with feeding increases. Our data suggest bumblebee nectar consumption was affected across the 50–200 μGy/hr range. We show field‐realistic radiation exposure influences fundamental metabolic processes with potential to drive changes in many downstream life‐history traits. We hypothesise that radiation may trigger energetically costly repair mechanisms, increasing metabolic rate and nectar requirements. This change could have significant ecological consequences in contaminated landscapes, including Chernobyl. We demonstrate bumblebees are more sensitive to radiation than assumed by existing international frameworks for environmental radiological protection. Read the free Plain Language Summary for this article on the Journal blog.