Rapid cell division defines evolutionary fitness for microorganisms but can be lethal during stress. Cells stop dividing under osmotic imbalance while adjusting their internal turgor pressure to the environment. Here we describe trade-offs between osmotic stress signaling, survival, and proliferation in a synthetic population of 50, ecologically distinct budding yeast. During rapid growth strong signaling predicted survival. Weak signaling predicted low viability, intense rebound signaling, and robust recovery. By contrast older cultures survived and adapted to unprecedented osmotic stress with fitness depending on reproducible, strain-specific proportions of cells with divergent signaling strategies. The most cautious cells survived extreme stress without dividing; the most reckless cells attempted to divide too soon and failed, killing both mother and daughter. A simple model with heritable proportions of cautious and reckless cells generates tunable, rapidly diversifying bet hedging strategies that resemble natural variation and would evolve in response to different patterns of osmotic stress.