Bone marrow fibrosis (BMF) develops in various hematologic and non-hematologic conditions and is a central pathological feature and major diagnostic criterion of myelofibrosis (MF). The cellular origin of BMF remains elusive, and novel cell-targeted therapeutics are needed. Here, we demonstrate using genetic fate tracing in two murine models of BMF that Gli1+ mesenchymal stromal cells (MSC) are recruited from the endosteal and perivascular niche to become fibrosis driving myofibroblasts of the bone marrow. We have sort-purified these cells and performed RNA sequencing