Sudden exposure to environmental stress threatens the viability of single-celled microbes and cells within complex tissues. In order to survive, cells must sense environmental changes and coordinate a transient cell cycle arrest with the appropriate adaptive response. Cells have several stress-responsive pathways that promote adaptation to distinct stressors, but how these pathways interact with one another is poorly understood. Here, we examined the response to calcium chloride stress, which activates the phosphatase calcineurin and the MAPK Hog1 in Saccharomyces cerevisiae. We discovered that calcineurin extends Hog1 activation, which causes prolonged downregulation of cell cycle-regulated genes and delays progression through multiple cell cycle phases. At the G1/S transition, crosstalk between calcineurin and Hog1 dramatically increases the duration of calcium-induced arrest. I found that Hog1 triggers arrest independent of calcineurin by decreasing G1 cyclin transcription and calcineurin maintains this arrest by extending Hog1-dependent activation of the G1 CDK inhibitor Cip1. These results suggest that stress-response pathway interactions tailor cell cycle arrest with adaptation to environmental stress. The immediate response to stress is well-characterized, but how cells maintain viability in challenging environments after recovering from a stress-induced arrest is unknown. I investigated the response to prolonged growth in calcium stress and found that calcineurin maintains fitness by promoting cell division and suppressing death. I determined that calcineurin helps cells proliferate and survive prolonged calcium exposure by two mechanisms, which differentially require a downstream transcription factor. Together, these findings highlight the importance of stress-response pathways during both acute and chronic environmental stress.