Updated project metadata. Ribosomes are produced in large quantities during oogenesis and stored in the egg. However, the egg and early embryo are translationally inactive. How translation is activated during embryogenesis is poorly understood. Using mass-spectrometry and cryo-EM analyses of ribosomes isolated from zebrafish and Xenopus eggs and embryos, we find that ribosomes transition from a dormant to an active state during the first hours of embryogenesis. Dormant ribosomes are associated with four factors that form two modules: a Habp4-eEF2 module that stabilizes ribosome levels and a Dap1b/Dapl1-eIF-5a module that represses translation. Dap/Dap1b is a newly discovered translational inhibitor that stably inserts into the polypeptide exit tunnel. Thus, a developmentally programmed, unique ribosome state plays a key role in ribosome storage and translational repression in the egg.