Gain or loss‐of‐function mutations in fibroblast growth factor receptor 3 (FGFR3) result in cranial vault defects highlighting the protein's role in membranous ossification. Zebrafish express high levels of fgfr3 during skull development;​ in order to study FGFR3's role in cranial vault development, we generated the first fgfr3 loss‐of‐function zebrafish (fgfr3^lof/lof). The mutant fish exhibited major changes in the craniofacial skeleton, with a lack of sutures, abnormal frontal and parietal bones, and the presence of ectopic bones. Integrated analyses (in vivo imaging and single‐cell RNA sequencing of the osteoblast lineage) of zebrafish fgfr3^lof/lof revealed a delay in osteoblast expansion and differentiation, together with changes in the extracellular matrix. These findings demonstrate that fgfr3 is a positive regulator of osteogenesis. We conclude that changes in the extracellular matrix within growing bone might impair cell–cell communication, mineralization, and new osteoblast recruitment.