The devastating blast fungus Magnaporthe oryzae elaborates invasive hyphae (IH) in living rice cells, separated from host cytoplasm by plant-derived interfacial membranes, but the molecular mechanisms and metabolic strategies (and hence metabolic vulnerabilities) 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 cycles of autophagy in IH modulate TOR reactivation via α-ketoglutarate to support biotrophic growth. Deleting the M. oryzae serine-threonine protein kinase-encoding gene RIM15 abolished the in planta autophagic cycling we describe here in wild type, attenuating biotrophic growth and disrupting interfacial membrane integrity. Δrim15 biotrophic growth was remediated by α-ketoglutarate treatment. Altogether, our results demonstrate that Rim15-dependent cycles of autophagic flux liberate α-ketoglutarate – via glutaminolysis – as an amino acid-sufficiency signal to trigger TOR reactivation and promote biotrophic growth in host rice cells.