Accumulating evidence demonstrates that fibroblasts play major roles in tissue development, homeostasis, wound healing and regeneration as well as in various pathologies. It is well accepted that significant intra-organ and inter-organ variations are evident within fibroblasts populations. Hence, the term ‘fibroblasts’ does not constitute one specific cell type but rather relates to heterogeneous groups of cells with distinct transcriptomes and distinct behaviors that are regulated differently during development, in diseased states or following injury. We have recently identified a small cluster of fibroblasts located near the muscle fiber termini that switch on a myogenic program and fuse into the developing muscles facilitating myotendinous junction development. With an aim at characterizing the fibroblasts, we have carried out single cell transcriptomal analysis of the developing muscles and identified the time points by which fibroblasts assume their identity. Notably, we find that not only do the fibroblasts differ in their transcriptional programs, but importantly they are also spatially restricted to unique regions within the muscle.