Acquired stress resistance (ASR) enables organisms to prepare for environmental changes that occur after an initial stressor. However, the genetic basis for ASR and how the underlying network evolved remain poorly understood. In this study, we discovered that a short phosphate starvation induces oxidative stress response (OSR) genes in the pathogenic yeast C. glabrata and protects it against a severe H2O2 stress; the same treatment, however, provides little benefit in the low pathogenic-potential relative, S. cerevisiae. This ASR involves the same transcription factors (TFs) as the OSR, but with different combinatorial logics. We show that Target-of-Rapamycin Complex 1 (TORC1) is differentially inhibited by phosphate starvation in the two species and contributes to the ASR via its proximal effector, Sch9. Therefore, evolution of the phosphate starvation-induced ASR involves the rewiring of TORC1's response to phosphate limitation and the repurposing of TF-target gene networks for the OSR using new regulatory logics. Author summary: Acquired Stress Resistance (ASR) is a phenomenon where mild stress makes an organism more resilient to subsequent severe stress. In this study, we uncovered a unique ASR in the opportunistic yeast pathogen C. glabrata compared to its less pathogenic relative S. cerevisiae. When subjected to a non-lethal phosphate starvation, C. glabrata activates genes that enhance its resistance to severe H2O2 stress, making it survive 3–10 times better than naïve cells, while the same treatment offers little to no protection in S. cerevisiae. We found that the underlying gene network for ASR shares key components with the typical oxidative stress response, but operates with different regulatory logics. Notably, the Target-of-Rapamycin Complex 1 (TORC1) responds differently to phosphate limitation in the two species, underpinning the species divergence in ASR. This discovery highlights a species-specific ASR and the key genetic factor driving the divergence. These findings shed light on how pathogenic yeasts adapt to their host environments. [ABSTRACT FROM AUTHOR]