Social thermoregulation is a means of maintaining homeostatic body temperature. While adult mice are a model organism for studying both social behavior and energy regulation, the relationship between huddling and core body temperature (Tb) is poorly understood. Here, we develop a behavioral paradigm and computational tools to identify active-huddling and quiescent-huddling as distinct thermal substates. We find that huddling is an effective thermoregulatory strategy in female but not male groups. At 23°C (room temperature), but not 30°C (near thermoneutrality), huddling facilitates large reductions in Tb and Tb-variance. Notably, active-huddling is associated with bidirectional changes in Tb, depending on its proximity to bouts of quiescent-huddling. Further, group-housed animals lacking the synaptic scaffolding gene Shank3b have hyperthermic Tb and spend less time huddling. In contrast, individuals lacking the cold-sensing gene Trpm8 have hypothermic Tb - a deficit that is rescued by increased huddling time. These results reveal how huddling behavior facilitates acute adjustments of Tb in a state-dependent manner.