Tolerance to desiccation in growing cultures of budding yeast (Saccharomyces cerevisiae) is inducible; only one in a million cells from a rapidly growing exponential culture survive desiccation compared to one in five cells from a stationary phase culture. Here, we exploit the desiccation sensitivity of exponentially dividing cells to understand both the relevant stresses imposed by desiccation and the stress response pathways that combat them. We found that the induction of desiccation tolerance is cell autonomous. We found an inverse correlation between desiccation tolerance and exponential growth rate in chemostats limited by glucose, ammonia or phosphate, as was reported previously for heat resistance. A transient heat shock prior to desiccation induces a five thousand-fold increase in desiccation tolerance in exponential phase cells. In contrast, prior hyper-ionic, reductive, oxidative, or hyperosmotic stress induces at most a 100-fold increase in desiccation tolerance. Furthermore, we provide evidence that the Sch9p regulated branch of the TOR pathway and the Ras-cAMP pathway controlled by Ras2p inhibit desiccation tolerance by inhibiting the stress response transcription factors Gis1p, Msn2p, and Msn4p and by activating Sfp1p, a transcription factor important for ribosome biogenesis. We discuss the implications of these new insights for the mechanism of desiccation tolerance and the potential for evolutionarily conservation of the regulation of this rare trait.