Muscle satellite cells are responsible for postnatal muscle growth and regeneration. Most skeletal muscles of the trunk and limb are derived from somites, but head muscles originate from cranial mesoderm. Here we first investigated the range of functional properties of satellite cells and then determined whether they were different in cells with separate embryonic origins, before examining how satellite cells respond to aging. Cultured satellite cells from head muscles proliferated more and differentiated later than those from limb muscles. Although some gene expression profiles in head‐derived satellite cells were different from limbs, head cells were able to regenerate limb muscles when transplanted. Surprisingly, clonal analysis showed that functional properties differed markedly between satellite cells: ranging from cells that proliferated extensively and gave rise to both differentiated and self‐renewed progeny, to other clones that divided only a few times before then differentiating completely. This heterogeneous distribution in satellite cell properties was preserved in both limb and head muscles from old mice. In conclusion, satellite cells exist as a functionally heterogeneous population, with many occupants of the satellite cell niche exhibiting stem cell characteristics in both somite‐derived and branchiomeric muscles. This study is supported by The Muscular Dystrophy Campaign.Grant Funding Source: Muscular Dystrophy Campaign. Medical Research Council. Wellcome Trust