Strategies to ensure fitness often slow organism development to delay reproduction and enhance survival. Across multiple organisms, reducing biosynthetic capacity results in developmental arrest early in life, but increased health- and lifespan post-developmentally. Here we demonstrate that these seemingly opposing responses are not an example of antagonistic pleiotropy; rather, we find that the nature of this developmental arrest is not sickness, but a regulated survival program responding to reduced cellular performance and mimicking a perceived reaction to toxin-producing pathogens, or otherwise, that can target eukaryotic protein synthesis. Early impairment of protein synthesis by targeting ribosome biogenesis (
rps-11/RPS11) or translation initiation (
egl-45/EIF3A) via RNAi, or ribosome progression via cycloheximide treatment, resulted in a specific arrest at larval stage 2 of C. elegans development, and C. elegans can survive in this state for periods that exceed their normal maximum lifespan. This arrest state is benign, as animals that recover can resume reproduction and live a normal lifespan. To protect animals in this pre-reproductive period, the arrest state affords resistance to thermal, oxidative, and heavy metal stress exposure. Although reduced protein synthesis results in cell-autonomous responses, reducing biosynthetic capacity via RNAi solely in the hypodermis was sufficient to initiate the organismal arrest state cell non-autonomously. We further show that loss of protein synthesis results in a reduction of pharyngeal pumping that is dependent upon AMPK-mediated signaling, which likely contributes to the increased longevity when protein synthesis is inhibited post-developmentally. Taken together, these data define the existence of a transient arrest-survival state initiated in response to a loss of protein biosynthesis and provide an evolutionary foundation for the conserved enhancement of healthy aging observed in post-developmental animals with reduced biosynthetic capacity.