ABSTRACT Skeletal muscle is the most widespread tissue in mammals and mediates several functions, and whose development is controlled by a coordinated transcriptional hierarchy that regulates the activities of a range of muscle genes. Skeletal muscle comprises various cells that create communication strategies for exchanging biological information. Nevertheless, the features and developmental programs of several of these cell lines remain unknown. We constructed a complete single‐cell landscape of prenatal to postnatal developing bovine skeletal muscle and compared its single‐cell transcriptomic characteristics with those of humans and mice. This landscape involved cellular heterogeneity, dynamic gene expression profiles, critical regulons during cell fate decisions, extensive networks of intercellular communication, and a gene regulation network. Overall, our results identify a developmental coordinate of the pluripotency spectrum among bovines, humans, and mice. This finding suggests evolutionary conservation and species‐specific differences in the skeletal muscle systems, extending to cell types, gene expression, and regulatory elements. These results offer insights into evolutionary conserved and divergent processes during mammalian skeletal muscle development.