Nutrient deprivation induces autophagy through inhibiting TORC1 activity. We describe a novel mechanism in Drosophila by which TORC1 regulates RNA processing of Atg transcripts and alters ATG protein levels and activities via the cleavage and polyadenylation (CPA) complex. We show that TORC1 signaling inhibits CDK8 and DOA kinases, which directly phosphorylate CPSF6, a component of the CPA complex. These phosphorylation events regulate CPSF6 localization, RNA binding, and starvation-induced alternative RNA processing of transcripts involved in autophagy, nutrient, and energy metabolism, thereby controlling autophagosome formation and metabolism. Similarly, we find that mammalian CDK8 and CLK2, a DOA ortholog, phosphorylate CPSF6 to regulate autophagy and metabolic changes upon starvation, revealing an evolutionarily conserved mechanism linking TORC1 signaling with RNA processing, autophagy, and metabolism. Display omitted •TORC1 negatively inhibits CDK8 and DOA kinases•CDK8 and DOA phosphorylate CPSF6 to induce alternative RNA processing•Depletion of CPSF6 impairs autophagy and metabolic changes during starvation•The CDK8-CLK2/DOA-CPSF6 axis is conserved in mammals Tang et al. investigate the mechanisms of how TORC1 regulates autophagy and cell metabolism. They demonstrate that CDK8 and DOA, two kinases downstream of TORC1 signaling, directly phosphorylate CPSF6 to regulate alternative mRNA polyadenylation and splicing and mediate TORC1-dependent physiological functions.