Regulation of alveolar fluid levels is essential for lung function. The amount and volume of the alveolar surface liquid (ASL) in the alveoli affects both, gas exchange and surfactant turnover. The mechanisms and the role of alveolar epithelial cells for maintaining alveolar fluid homeostasis are still controversial. We have recently described that exocytosis of lamellar bodies (LBs) in primary alveolar type II (ATII) epithelial cells results in “fusion-activated cation-entry” (FACE) via P2X₄ receptors on LBs. Here we demonstrate that FACE, in addition to facilitating surfactant secretion, modulates alveolar fluid transport. Correlative fluorescence and atomic force microscopy revealed that FACE-dependent water influx correlated with individual fusion events in ATII cells. Moreover, ATII cell monolayers grown at air-liquid-interface exhibited increases in short-circuit current (I_sc) upon stimulation with ATP or UTP. Both are potent agonists for LB exocytosis, but only ATP activates FACE. ATP, not UTP, elicited additional fusion-dependent increases in I_sc. Over-expressing dominant-negative P2X₄ abrogated this effect by ~ 50%, whereas potentiating P2X₄ lead to ~ 80% increase in I_sc. In a more direct approach, we directly monitored changes in ASL on ATII monolayers by confocal microscopy. Only stimulation with ATP, not UTP, led to a significant, fusion-dependent, 20% decrease in ASL, indicating apical-to-basolateral fluid transport across ATII monolayers. Finally, our findings were confirmed in in situ measurements of changes in lung compliance upon stimulation of LB fusion and activation of FACE. In summary, our data support a new concept where fluid resorption in the alveolus is directly coupled to surfactant secretion.