Precise developmental control of jaw length is critical for survival, but underlying molecular mechanisms remain poorly understood. The jaw skeleton arises from neural crest mesenchyme (NCM), and we previously demonstrated that these progenitor cells express more bone-resorbing enzymes including Matrix metalloproteinase 13 (Mmp13) when they generate shorter jaws in quail embryos versus longer jaws in duck. Moreover, if we inhibit bone resorption or Mmp13, we can increase jaw length. In the current study, we uncover mechanisms establishing species-specific levels of Mmp13 and bone resorption. Quail show greater activation of, and sensitivity to Transforming Growth Factor-Beta (TGFβ) signaling than duck; where mediators like SMADs and targets like Runx2, which bind Mmp13, become elevated. Inhibiting TGFβ signaling decreases bone resorption and overexpressing Mmp13 in NCM shortens the duck lower jaw. To elucidate the basis for this differential regulation we examine the Mmp13 promoter. We discover a SMAD binding element and single nucleotide polymorphisms (SNPs) near a RUNX2 binding element that distinguish quail from duck. Altering the SMAD site and switching the SNPs abolishes TGFβ-sensitivity in the quail Mmp13 promoter but makes the duck promoter responsive. Thus, differential regulation of TGFβ signaling and Mmp13 promoter structure underlie avian jaw development and evolution.