The osteopetrosis associated with colony stimulating factor 1 (Csf1) and Csf1 receptor (Csf1r) mutations has been primarily attributed to the loss of osteoclasts and deficiency in bone resorption. The rodent Csf1r knockout (Csf1rko) phenotype is more severe, with postnatal lethality common, restricting opportunity to study impacts on postnatal skeletal development. We recently characterized delayed postnatal skeletal ossification in an inbred homozygous Csf1rko rat model that survives into adulthood and that this could be rescued by intraperitoneal cell transfer of whole bone marrow (BMT) without donor-derived haematopoietic conversion (1). Here, we have examined the cellular basis for the skeletal phenotype in the Csf1rko rat up to 7 weeks of age and myeloid cell dynamics associated with BMT rescue. We verified continuing osteoclasts deficiency in Csf1rko rat bones that was associated with persistent ineffective removal of growth plate primary spongiosa, ineffective remodelling of woven bone in spongiosa and failed excavation of the medulla. Osteogenesis at secondary ossification centres (SOC) and sites of subarticular ossification was delayed in Csf1rko rats but not stalled with notable progression observed between 3-7 weeks of age. Temporal micro-CT and in situ analysis indicated that at these anatomical sites in control rats, osteomac infiltration preceded osteoclasts during excavation of the cartilage anlagen. Interestingly, breakthrough re-emergence of osteomacs in Csf1rko corresponded with delayed ossification initiation. Accelerated phenotype reversal following BMT in Csf1rko rats was characterised by osteomacs acting as pioneering cells at all sites of ossification. Osteomacs persisted throughout phenotype reversal, being juxtaposition to both osteoblast and osteoclast at sites of elevated bone remodelling/modelling. Osteomac and osteoclast repopulation persisted at least 5 weeks post-BMT, suggesting prolonged engraftment of non-haematopoiesis-derived precursors within the peritoneum and/or throughout the skeleton. These observations extend evidence that osteomacs independently contribute to bone dynamic events underpinning normal postnatal bone growth and morphogenesis.