Stress tolerance and rapid growth are often competing interests in cells. Upon severe environmental stress, many organisms activate defense systems concurrent with growth arrest. There has been debate as to whether aspects of the stress-activated transcriptome are regulated by stress or an indirect byproduct of reduced proliferation. For example, stressed Saccharomyces cerevisiae cells mount a common gene expression program called the environmental stress response (ESR) [1] comprised of ∼300 induced (iESR) transcripts involved in stress defense and ∼600 reduced (rESR) mRNAs encoding ribosomal proteins (RPs) and ribosome biogenesis factors (RiBi) important for division. Because ESR activation also correlates with reduced growth rate in nutrient-restricted chemostats and prolonged G1 in slow-growing mutants, an alternate proposal is that the ESR is simply a consequence of reduced division [2-5]. A major challenge is that past studies did not separate effects of division arrest and stress defense; thus, the true responsiveness of the ESR-and the purpose of stress-dependent rESR repression in particular-remains unclear. Here, we decoupled cell division from the stress response by following transcriptome, proteome, and polysome changes in arrested cells responding to acute stress. We show that the ESR cannot be explained by changes in growth rate or cell-cycle phase during stress acclimation. Instead, failure to repress rESR transcripts reduces polysome association of induced transcripts, delaying production of their proteins. Our results suggest that stressed cells alleviate competition for translation factors by removing mRNAs and ribosomes from the translating pool, directing translational capacity toward induced transcripts to accelerate protein production.