The devastating blast fungus Magnaporthe oryzae elaborates invasive hyphae (IH) in living rice cells during early infection, separated from host cytoplasm by plant-derived interfacial membranes, but the metabolic strategies underpinning this fundamental intracellular biotrophic growth phase are poorly understood. Eukaryotic cell growth depends on activated target-of-rapamycin (TOR) kinase signaling, which inhibits autophagy. Here, using live-cell imaging coupled with multiomic approaches, we show how the M. oryzae serine/threonine protein kinase Rim15 coordinates cycles of autophagy and glutaminolysis in IH – the latter through phosphorylation of NAD-dependent glutamate dehydrogenase – to reactivate TOR and promote biotrophic growth. Deleting RIM15 attenuated IH growth and triggered plant immunity; these defects were fully remediated by exogenous α-ketoglutarate treatment, but glucose treatment only suppressed host defenses. Our results together suggest that Rim15-dependent cycles of autophagic flux liberate α-ketoglutarate – via glutaminolysis – to reactivate TOR signaling and fuel biotrophic growth while conserving glucose for antioxidation-mediated host innate immunity suppression.