Whether or not a cell chooses to divide is a tightly regulated and extremely important decision. Cells from yeast to human are able to reversibly exit the cell cycle in response to environmental changes such as nutritional changes or removal of growth cues to become quiescent. An inappropriate response to environmental cues can result in overproliferation which can lead to cancer, or a failure to proliferate which can result in developmental defects, premature aging and defects in wound healing. While many of the cell signaling pathways involved in regulating cellular quiescence have been identified, how these pathways translate their messages into transcriptional outputs is not well characterized. We previously showed that the histone deacetylase Rpd3 mediates global histone deacetylation and transcription repression upon quiescence entry. How the activation of quiescence-specific genes occurs in the midst of this transcriptionally repressive environment is not well understood. We show that the SWI/SNF chromatin remodeling complex activates quiescence specific genes to promote entry into quiescence. We additionally show that SWI/SNF binding early during quiescence entry is important for facilitating localization of the transcriptional activator Gis1, as well as histone H4 hypoacetylation in coding regions later on. The increase in H4 acetylation that we observe at Snf2-regulated genes upon Snf2 depletion corresponds to a decrease in promoter-bound Rpd3, suggesting that Snf2 remodels chromatin not only to facilitate activator binding, but also the binding of Rpd3. These observations provide mechanistic insight as to how quiescence-specific genes can be activated in the face of global deacetylation and transcription repression.