Increasingly frequent warm periods during winter, which are associated with climate change, may cause mismatches between the colony phenology of the western honey bee, Apis mellifera L., and their floral resources. Warmer winter periods can also affect colony brood rearing activity and consequently the reproduction of the invasive brood parasite Varroa destructor Anderson and Trueman. Until now little is known about the effects of climate change on biotic interactions in such a multitrophic system comprising flowering plants, a pollinator, and its parasite. We performed a reciprocal translocation experiment with honey bee colonies to simulate climate change-induced phenology shifts. Honey bee brood phenology was highly sensitive to environmental conditions in late winter. Colonies in which phenology was experimentally delayed had smaller worker populations in early spring and reduced amounts of stored honey during the following months. During summer, the varroa load in colonies with non-shifted phenology was three times higher than in colonies with delayed phenology. High varroa loads during summer were negatively correlated with worker population growth. Despite a remarkable resilience of colony development to phenology shifts, our results show that mismatches between the phenology of honey bee colonies and flowering plants can affect the build-up of resource stores. Further, an advanced onset of brood rearing activity after hibernation can reinforce the negative impact of the brood parasite V. destructor. We conclude that trade-offs between synchronisation with earlier flower phenology and prolonged brood phases with build-up of varroa populations might constrain the honey bees' capability to adapt to climate warming.