The scarcity of soil phosphorus (P), an essential macronutrient, often limits plant growth and development. Enhanced secretion of intracellular and secretory acid phosphatases is essential to maintain cellular inorganic P (Pi) homeostasis in plants. Herein, using transcriptomics and proteomics approach, we observed upregulation of several purple acid phosphatases (PAPs), includingSlPAP1,SlPAP10b,SlPAP12,SlPAP15,SlPAP17b,SlPAP26a, andSlPAP26bin Pi-deficient tomato seedlings. Higher transcript levels ofSlPAP17bandSlPAP26bin the older senescing leaves than the younger leaves indicated active involvement of these PAPs in Pi remobilization. Subsequent detailed characterization ofSlPAP17b,SlPAP26a, andSlPAP26brevealed a prominent role ofSlPAP26bin Pi homeostasis. Silencing ofSlPAP26bled to an exacerbated P starvation response as these plants exhibited smaller shoots, lower soluble Pi, total P levels, and higher sucrose than their EV controls under Pi deprivation.SlPAP26b-silenced plants also showed misregulation of P starvation inducible genes such as phosphate transporters and glycerolipid remodellers, even under Pi-sufficient conditions. WhereasSlPAP26blevels were induced by external sucrose, its expression was found to be independent of the Myb class master regulators of P starvation response, SlPHR1 and SlPHL1. Altogether, this study identifies a prominent role ofSlPAP26bin the Pi compensation network in tomato seedlings.