Yeast perceive and respond to changes in their external environment by rapidly modulating its transcriptional program. A core set of genes are upregulated and repressed under several stresses examined. These genes are under the transcriptional control of the stress responsive factor Msn2. Single cell microscopy studies revealed that Msn2 re-localizes from the cytoplasm to the nucleus when cells are stressed. This change in localization is dynamic, which is observed by the presence of short-lived random bursts of Msn2 nuclear occupancy. We observed that Msn2 localization was uniquely modulated for different stresses. We investigated the consequence of this dynamic behavior of Msn2 on transcription of genes using microarrays. Ectopic expression of transient and prolonged nuclear Msn2 forms led to differential gene expression kinetics. Some genes were readily induced i.e fast responding and others required a constant nuclear presence of Msn2. This suggests that by modulating transcription factor dynamics yeast can selectively regulate gene expression depending on the stressor. Whole genome chromatin immunoprecipitation and nucleosome positioning studies post nutrient downshift and oxidative stress corroborated our findings and we observed Msn2 binding to promoters of common stress regulated genes as well as genes pertaining to the stressor. Isogenic cells also responded to stress distinctly, with some cells showing prolonged nuclear accumulation of Msn2 and others a more transient phenotype. Overexpression of constitutively nuclear phospho-mutant Msn2 causes cells to undergo cell-cycle arrest, suggesting a direct role for Msn2 in cell growth. Our studies elucidate the complex and inter-dependent mechanisms underlying gene expression changes and the process of “bet hedging” which occurs during stress.