Within the same species of eusocial insects, individuals of different castes typically display widely different life-history traits: sterile workers live for a few months, while queens can live for decades. Aging theories emphasise the importance of metabolism and oxidative stress in explaining longevity, with mitochondrial bioenergetics standing at the crossroads of energy and reactive oxygen species production. The study of mitochondrial functioning is therefore of great relevance in determining the nature of the mechanisms that explain the contrasting longevities between insect social castes. We addressed this question in the eusocial black garden ant Lasius niger. Our findings reveal that caste differences in mitochondrial bioenergetics and the oxidative balance only partially align with oxidative stress theory predictions. Long-lived queens display lower metabolic rates and mitochondrial density, yet maintaining higher cellular energy availability, as reflected by a high adenylate energy charge (AEC). This may result from enhanced mitochondrial maintenance processes and specific recourse to the purine salvage pathway, promoting ATP availability while limiting oxidative cost. This perspective highlights the unique bioenergetic adaptations that may be behind the queens’ remarkable lifespan.