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Cellular transitions require dramatic changes in gene expression that are supported by regulated mRNA decay and new transcription. The maternal‐to‐zygotic transition is a conserved developmental progression during which thousands of maternal mRNAs are cleared by post‐transcriptional mechanisms. Although some maternal mRNAs are targeted for degradation by microRNAs, this pathway does not fully explain mRNA clearance. We investigated how codon identity and translation affect mRNA stability during development and homeostasis. We show that the codon triplet contains translation‐dependent regulatory information that influences transcript decay. Codon composition shapes maternal mRNA clearance during the maternal‐to‐zygotic transition in zebrafish, Xenopus, mouse, and Drosophila, and gene expression during homeostasis across human tissues. Some synonymous codons show consistent …