Cells stabilize intracellular inorganic phosphate (P _i ) to compromise between large biosynthetic needs and detrimental bioenergetic effects of P _i . P _i homeostasis in eukaryotes uses Syg1/Pho81/Xpr1 (SPX) domains, which are receptors for inositol pyrophosphates. We explored how polymerization and storage of P _i in acidocalcisome-like vacuoles supports Saccharomyces cerevisiae metabolism and how these cells recognize P _i scarcity. Whereas P _i starvation affects numerous metabolic pathways, beginning P _i scarcity affects few metabolites. These include inositol pyrophosphates and ATP, a low-affinity substrate for inositol pyrophosphate-synthesizing kinases. Declining ATP and inositol pyrophosphates may thus be indicators of impending P _i limitation. Actual P _i starvation triggers accumulation of the purine synthesis intermediate 5-aminoimidazole-4-carboxamide ribonucleotide (AICAR), which activates P _i -dependent transcription factors. Cells lacking inorganic polyphosphate show P _i starvation features already under P _i -replete conditions, suggesting that vacuolar polyphosphate supplies P _i for metabolism even when P _i is abundant. However, polyphosphate deficiency also generates unique metabolic changes that are not observed in starving wild-type cells. Polyphosphate in acidocalcisome-like vacuoles may hence be more than a global phosphate reserve and channel P _i to preferred cellular processes. IMPORTANCE Cells must strike a delicate balance between the high demand of inorganic phosphate (P _i ) for synthesizing nucleic acids and phospholipids and its detrimental bioenergetic effects by reducing the free energy of nucleotide hydrolysis. The latter may stall metabolism. Therefore, microorganisms manage the import and export of phosphate, its conversion into osmotically inactive inorganic polyphosphates, and their storage in dedicated organelles (acidocalcisomes). Here, we provide novel insights into metabolic changes that yeast cells may use to signal declining phosphate availability in the cytosol and differentiate it from actual phosphate starvation. We also analyze the role of acidocalcisome-like organelles in phosphate homeostasis. This study uncovers an unexpected role of the polyphosphate pool in these organelles under phosphate-rich conditions, indicating that its metabolic roles go beyond that of a phosphate reserve for surviving starvation.