Cilia at the node generate a leftward fluid flow that breaks left-right symmetry. However, the molecular mechanisms that regulate ciliogenesis at the node are largely unknown. Here, we show that the epiblast-specific deletion of the gene encoding the BMP type 1 receptor (Acvr1) compromised development of nodal cilia, which results in defects in leftward fluid flow and, thus, abnormalities in left-right patterning. Acvr1 deficiency in mouse embryonic fibroblasts (MEFs) resulted in severe defects in their quiescence-induced primary cilia. Although the induction of quiescence in wild-type MEFs leads to an increase in the level of the cyclin-dependent kinase inhibitor p27Kip1 and to rapid p27Kip1 phosphorylation on Ser10, MEFs deficient in Acvr1 show a reduction in both p27Kip1 protein levels and in p27Kip1 Ser10 phosphorylation. The observed defects in cilium development were rescued by the introduction of p27Kip1 into Acvr1-deficient MEFs, implying that BMP signaling positively controls p27Kip1 stability in the G0 phase via p27Kip1 Ser10 phosphorylation, which is a prerequisite for induction of primary cilia. Importantly, in control embryos, p27Kip1 protein is clearly present and strongly phosphorylated on Ser10 in cells on the quiescent ventral surface of the node. By contrast, the corresponding cells in the node of Acvr1 mutant embryos were proliferative and showed a dramatic attenuation in both p27Kip1 protein levels and phosphorylation on Ser10. Our data suggest that cell quiescence controlled by BMP signaling via ACVR1 is required for transient formation of nodal cilia, and provide insight into the fundamental question of how the node represents the mechanistic `node' that regulates the development of left-right symmetry in vertebrates.