For decades, the honeybee, Apis mellifera, has suffered from severe colony losses due to the ectoparasitic mite Varroa destructor. Various strategies based on chemicals fail to adequately control varroa mite populations, and often comprise side-effects on the host, parasite resistance and residues in hive products. Reduced temperature tolerance of V. destructor compared to its host has long been recognised and accordingly, the potential of hyperthermia to disrupt mite reproduction within honeybee brood cells or even kill adult parasites. Yet, earlier studies on hyperthermia remain largely anecdotal, and readily implementable solutions have so far been lacking. This study investigates autonomously controlled interval heating from within brood combs throughout the season compared to control colonies maintained according to good apicultural practice. We documented treatment-dependent colony growth dynamics and honey production at three apiaries, complemented by regular monitoring of varroa mite levels and comprehensive digital assessments of brood development over time. Our one-year field trial suggests the evaluated hyperthermia device efficiently suppresses mite populations below critical thresholds until autumn. Whilst a general winter reference-curing revealed similar mite infestations of colonies previously treated with hyperthermia versus formic acid (control), only the latter imposed substantial overwintering burdens indirectly through frequent late-season queen supersedure. However, relative to targeted pupae, increased mortality particularly of heat-treated non-target brood stages (eggs and larvae) appeared to trigger compensatory colony-level responses, translating into temporarily decreased numbers of adult workers coupled with increased pollen foraging and overall lower honey harvests. Valuable insights into previously unrecognised side-effects of hyperthermia and mitigation thereof may ultimately permit successful routine applications of this chemical-free approach to combat the major threat to honeybees worldwide.