The developmental origin of adipose tissue and what controls its distribution is poorly understood. By lineage tracing and gene expression analysis in mice, we provide evidence that mesenchymal precursors expressing Myf5—which are thought to give rise only to brown adipocytes and skeletal muscle—also give rise to a subset of white adipocytes. Furthermore, individual brown and white fats contain a mixture of adipocyte progenitor cells derived from Myf5⁺ and Myf5^neg lineages, the number of which varies with depot location. Subsets of white adipocytes originating from both Myf5⁺ and Myf5^neg precursors respond to β₃-adrenoreceptor stimulation, suggesting "brite" adipocytes may also have multiple origins. We additionally find that deleting PTEN with myf5-cre causes lipomatosis and partial lipodystrophy by selectively expanding the Myf5⁺ adipocyte lineages. Thus, the spectrum of adipocytes arising from Myf5⁺ precursors is broader than previously thought, and differences in PI3K activity between adipocyte lineages alter body fat distribution.