miR-31 is an evolutionary conserved microRNA that has been studied in myogenesis, skeletogenesis and cancer; however, the role of miR-31, and microRNAs in general, in post-transcriptional regulation during development is not as well studied. Here, Jia Song and colleagues uncover the role of miR-31 in mitosis regulation during early embryogenesis in sea urchins. First, the authors observe that miR-31 is localised to the mitotic spindles in a cell cycle-dependent manner. Inhibiting miR-31 in embryos leads to developmental delay and defects in the cytoskeleton and chromosomal segregation. Then, the authors identify several miR-31 target transcripts, including β-actin, Rab35 and Fascin, which encode regulators of cytoskeleton dynamics. They find that miR-31 and its targets co-localise at the mitotic spindle during mitosis. Inhibiting miR-31 results in more newly translated Fascin at the spindle. Moreover, the authors find that ectopic Fascin mRNA localisation and translation at the cell membrane leads to developmental defects. Finally, the authors also observe co-localisation of miR-31 and its targets, and active Fascin translation at the mitotic spindle in mammalian cells, suggesting the role of miR-31 at the spindle could be evolutionarily conserved. Overall, the findings suggest that miR-31 regulates local translation of cytoskeletal remodelling transcripts at the mitotic spindle to ensure proper cell division during embryogenesis.