Skeletal and joint morphogenesis is regulated in large part by modulation of the bone morphogenetic protein (BMP) signaling pathway and its component parts. Activating mutations in the Type I BMP receptor ACVR1 cause fibrodysplasia ossificans progressiva (FOP), a disease of heterotopic ossification that is heralded at birth by a signature malformation of the first digit of the hindlimb. We used mouse models of FOP together with patient radiographic data to interrogate the role ACVR1 plays in the morphology and development of the skeleton. Focusing on the digits in Acvr1R206H/+;Prrx1-Cre mice, we identified reduced restriction of the BMP pathway upstream of improper specification of mesenchymal joint progenitor cells and aberrant chondrogenesis in digit joints, leading to joint agenesis and developmental delay. Of note, specific joints were more severely affected than others. Our analysis of patient data identified previously underappreciated phenotypes of skeletal dysmorphia and degenerative arthropathy in FOP patients at specific, clinically relevant anatomical sites. These data support a role for ACVR1 in site-specific regulation of joint development and health and broaden our understanding of the endogenous skeletal phenotype of FOP, providing new insights and clarity to BMP signaling in development and into this rare disease.