Tuberous Sclerosis Complex (TSC) is caused by mutations in *TSC1* or *TSC2* genes, leading to hyperactivation of mTORC1 and organ lesions, particularly in the kidney. Previous studies have shown that TFEB is constitutively active in TSC. In this study, we generated two mouse models of TSC with a primary focus on kidney pathology. Knockout of TFEB rescued kidney pathology and improved survival, indicating that TFEB is the primary driver of renal disease in TSC. Importantly, increased mTORC1 activity in TSC2-deficient kidneys was normalized by TFEB knockout. In TSC2-deficient cells, Rheb knockdown or Rapamycin treatment paradoxically increased TFEB phosphorylation at the mTORC1 sites and relocalized TFEB from the nucleus to the cytoplasm. Rapamycin treatment in mice normalized lysosomal gene expression, similar to TFEB knockout, suggesting that Rapamycin's benefit in TSC is TFEB-dependent. These findings change the understanding of mTORC1 hyperactivation in TSC and may lead to therapeutic strategies.Tuberous Sclerosis Complex (TSC) is caused by mutations in *TSC1* or *TSC2* genes, leading to hyperactivation of mTORC1 and organ lesions, particularly in the kidney. Previous studies have shown that TFEB is constitutively active in TSC. In this study, we generated two mouse models of TSC with a primary focus on kidney pathology. Knockout of TFEB rescued kidney pathology and improved survival, indicating that TFEB is the primary driver of renal disease in TSC. Importantly, increased mTORC1 activity in TSC2-deficient kidneys was normalized by TFEB knockout. In TSC2-deficient cells, Rheb knockdown or Rapamycin treatment paradoxically increased TFEB phosphorylation at the mTORC1 sites and relocalized TFEB from the nucleus to the cytoplasm. Rapamycin treatment in mice normalized lysosomal gene expression, similar to TFEB knockout, suggesting that Rapamycin's benefit in TSC is TFEB-dependent. These findings change the understanding of mTORC1 hyperactivation in TSC and may lead to therapeutic strategies.