Food shortages and infectious diseases were constant threats throughout mammalian evolution and often occurred simultaneously. When food availability is reduced, it is unclear how the host adapts to support glucose-demanding immune processes while preventing hypoglycemia. In the context of dietary restriction (DR), we found that glucocorticoids (GCs) aligned naive, effector, and memory T cell populations with the nutritional status of the host. DR-induced GCs promoted naive T cell homing to the bone marrow, which supported their homeostasis at steady state. Following a primary infection, DR-induced GCs rewired immunity to simultaneously uphold pathogen control and systemic glucose homeostasis. GCs achieved this by dampening effector T cells and enhancing the response of neutrophils with reduced glucose dependence. Although the total effector T cell pool was decreased during DR, GCs enriched memory-precursor effector cells to preserve memory formation. Thus, GCs align immunity and metabolic physiology to ensure host fitness when food availability is reduced.