Phenotypic plasticity is thought to be of prime importance for the evolution of castes in social insects. However, conclusions are generally drawn from holometabolous social Hymenoptera, whereas little is known about the hemimetabolous termites. We investigated the influence of environmental conditions on the expression of the alternative phenotypes, worker versus dispersing sexual, in the drywood termite Cryptotermes secundus. Season played a fundamental role in this regulatory process by setting developmental deadlines. Individuals failing to reach these deadlines developed back to workers, whereas those in time progressed to dispersing sexuals. This seasonal regulation was superposed by the influence of food availability in the nest that adjusted the number of remaining workers versus dispersing sexuals. In line with declining benefits at the natal nest, there were more dispersing sexuals when the food was reduced. Provided that the life type of C. secundus reflects the ancestral state in termite evolution, as is often assumed, our results support the hypothesis that termite workers originated from individuals failing in sexual development. Furthermore, a taxonomical comparison between termite species with different life-styles stresses the importance of a predictable variation in food availability for the existence of a plastic development and the occurrence of conditionally expressed phenotypes in termites. Compared with social Hymenoptera, the mechanisms involved in caste polyphenism in termites differed considerably, which demands more differentiated discussions about social insects caste polyphenism.