Specialized defence traits and strategies are crucial in surviving enemy attacks and in resource acquisition. In numerous social insect lineages, soldiers function as specialized defence traits of the colony, but associated defence strategies are poorly known. The turtle ant Cephalotes rohweri is an obligate cavity-nesting ant with highly specialized soldiers. To maximize growth and reproduction, colonies must use their limited availability of soldiers to defend multiple cavities. Using laboratory experiments informed by field data, we addressed how soldier ‘deployment’ across cavities adjusts to changes in cavity availability and quality. From initial field-like conditions, soldier deployment to newly available cavities was rapid, stabilized quickly, and at least doubled the number of cavities defended by each colony. New cavities were defended by fewer soldiers than original cavities still in use. Nevertheless, when new cavities differed in size, an important quality metric, large cavities were used more often and defended by more soldiers than small cavities. Despite these dynamic responses, total soldier deployment to new cavities was limited to an approximately constant proportion (0.4) of overall soldier availability across colonies and resource contexts. Moreover, there was a significant positive relationship between total soldier deployment to new cavities (greater for larger colonies) and both the number of newly defended cavities and their average level of defence. These results demonstrate that colony-wide soldier deployment is dynamic, predictable and context sensitive but ultimately constrained by the availability of soldiers in the colony. Furthermore, the consistently lower number of soldiers in new cavities, which always limits the potential losses to enemies, is concordant with a ‘conservative bet-hedging’ life history strategy. Broadly, our findings show that a specialized soldier caste can be associated with a far more sophisticated defence strategy than previously recognized. This provides a more complete perspective on the evolution of soldier-based defences in insect societies.