Nutrient availability governs growth and quiescence, and many animals arrest development when starved. Using C. elegans L1 arrest as a model, we show that gene expression changes deep into starvation. Surprisingly, relative expression of germline-enriched genes increases for days. We conditionally degrade the large subunit of RNA polymerase II using the auxin-inducible degron system and analyze absolute expression levels. We find that somatic transcription is required for survival, but the germline maintains transcriptional quiescence. Thousands of genes are continuously transcribed in the soma, though their absolute abundance declines, such that relative expression of germline transcripts increases given extreme transcript stability. Aberrantly activating transcription in starved germ cells compromises reproduction, demonstrating important physiological function of transcriptional quiescence. This work reveals alternative somatic and germline gene-regulatory strategies during starvation, with the soma maintaining a robust transcriptional response to support survival and the germline maintaining transcriptional quiescence to support future reproductive success. Display omitted •Gene expression changes for the duration of starvation-induced developmental arrest•Somatic transcription is required early, but not late, to support starvation survival•The germline remains transcriptionally quiescent, supporting future reproduction•Germline transcripts are exceptionally stable compared to somatic transcripts Webster et al. show that the transcriptional response to starvation is mounted early in larval somatic cells supporting survival but that it wanes over time. In contrast, they show that the germline remains transcriptionally quiescent deep into starvation, supporting reproductive potential, while maintaining its transcriptome via transcript stability.