Craniofacial development is a complex morphogenic process that requires highly orchestrated interactions between multiple cell types. Blood vessel-derived angiocrine factors are known to promote proliferation of chondrocytes in Meckel's cartilage to drive jaw outgrowth, however the specific factors controlling this process remain unknown. Here, we use in vitro and ex vivo cell and tissue culture, as well as genetic mouse models to identify IGF-1 as a novel angiocrine factor directing Meckel's cartilage growth during embryonic development. We show that IGF-1 is secreted by blood vessels and that deficient IGF-1 signalling underlies mandibular hypoplasia in Wnt1-Cre; Vegfafl/fl mice that exhibit vascular and associated jaw defects. Furthermore, conditional removal of IGF-1 from blood vessels causes craniofacial defects including a shortened mandible, and reduced proliferation of Meckel's cartilage chondrocytes. This demonstrates a critical angiocrine role for IGF-1 during craniofacial cartilage growth, and identifies IGF-1 as a putative therapeutic for jaw and/or cartilage growth disorders.