Insect diapause represents an evolutionarily conserved developmental arrest strategy characterized by profound metabolic suppression, though its underlying regulatory mechanisms remain incompletely elucidated. In this study, we identify a crucial signaling cascade involving transforming growth factor β receptor I (TGFβRI), atypical protein kinase C (aPKC), and phosphoenolpyruvate carboxykinase (PEPCK) that orchestrates metabolic reprogramming during pupal diapause in Helicoverpa armigera. Temporospatial expression profiling revealed coordinated downregulation of TGFβRI and PEPCK, a key gluconeogenic enzyme in diapause-destined pupae. Overexpression of TGFβRI was found to increase PEPCK levels in Helicoverpa zea ovarian cells (HzAm1). Concordantly, treatment of nondiapause-destined pupae with SB431542, a TGFβRI inhibitor, suppressed PEPCK in a dose-dependent manner. Further analysis revealed that aPKC serves as a downstream effector, as its phosphorylation levels were notably elevated in nondiapause-destined pupae, corresponding to TGFβRI activity. Notably, TGFβRI selectively regulates aPKC phosphorylation without altering total protein levels. Disrupting aPKC, either through RNAi-mediated knockdown or pharmacological inhibition (Go6983), robustly diminished PEPCK expression both in vitro and in vivo, and crucially delayed pupal development. Evolutionary analysis uncovered 50–70% sequence conservation of aPKC across Lepidoptera, highlighting its regulatory significance. Taken together, our findings elucidate a TGFβRI/aPKC/PEPCK axis that couples developmental signaling with metabolic regulation during insect diapause, offering mechanistic insights into this adaptive survival strategy.