Eusocial insects operate as an integrated collective with tasks allocated among individuals. This applies also to reproduction, through coordinated mating flights between male and female reproductives. While in some species male sexuals take only a single mating flight and never return, in the Western honey bee, Apis mellifera, the male sexuals (drones) live in the colony throughout their lives. Prior research has focused almost exclusively on drone behavior outside of the nest (mating flights), while ignoring the majority of their life, which is spent inside the nest. To understand the in-nest behavior of drones across their lives, we used the BeesBook tracking system to track 192 individually-marked drones continuously for over 20 days, to examine how drones moved and spent time in the nest. In agreement with previous work, we find that drones spend most of their time immobile at the nest periphery. However, we also observe that drones have periods of in-nest hyperactivity, during which they become the most active individuals in the entire colony. This in-nest hyperactivity develops in drones after age 7 days, occurs daily in the afternoon, and coincides with drones taking outside trips. We find strong synchronization across the drones in the start/end of activity, such that the drones in the colony exhibit a “shared activation period”. The duration of the shared activation period depends on the weather; when conditions are suitable for mating flights, the activation period is extended. At the individual-level, we see that the activation order changes from day to day, suggesting that both the external influence of weather conditions, as well as exchange of social information, influences individual activation. Using an accumulation-to-threshold model of drone activation, we show that simulations using social information match experimental observations. These results provide new insight into the in-nest behavior of drones, and how their behavior reflects their role as the male gametes of the colony.