Guttation, the formation of exudation water, is widespread among plants and fungi, yet the underlying mechanisms remain largely unknown. We describe the conditions for inducing guttation in sporangiophores of the mucoracean fungus, Phycomyces blakesleeanus. Cultivation on peptone-enriched potato dextrose agar elicits vigorous guttation mainly below the apical growing zone, while sporangiophores raised on a glucose-mineral medium manifest only moderate guttation. Mycelia do not guttate irrespective of the employed media. The topology of guttation droplets allows identifying the non-growing part of the sporangiophore as a guttation zone, which responds to humidity and medium composition in ways that become relevant for turgor homeostasis and thus the sensor physiology of the growing zone. Apparently, the entire sporangiophore, rather than exclusively the growing zone, participates in signal reception and integration to generate a common growth output. Exogenous auxin applied to the growing zones elicits two correlated responses: (i) formation of guttation droplets in the growing and transition zones below the sporangium and (ii) a diminution of the growth rate. In sporangiophore populations, guttation-induction by exogenous control buffer occurs at low frequencies; the bias for guttation increases with increasing auxin concentration. Synthetic auxins and the transport inhibitor NPA suppress guttation completely, but leave growth rates largely unaffected. Mutants C2 carA and C148 carA madC display higher sensitivities for auxin-induced guttation compared to wild type. A working model for guttation includes aquaporins and mechanosensitive ion channels that we identified in Phycomyces by sequence domain searches.