The parathyroid glands regulate blood calcium homeostasis through the secretion of parathyroid hormone. In mice, the parathyroid develops together with thymus in the third pharyngeal pouch. When these organs separate, cervical thymi and ectopic parathyroids are deposited in the neck. Parathyroid-derived cervical thymi arise when parathyroid cells spontaneously turn off the parathyroid program and transdifferentiate to a thymus fate. Occurring at a low frequency and increasing steadily until birth, this fate switch reveals the unstable differentiation program of fetal parathyroid cells. The molecular mechanism governing parathyroid cell fate instability is unclear. We hypothesized that the low proliferation rate of parathyroid cells may be a source of lineage instability. Our findings indicate that driving parathyroid cell proliferation stabilizes the parathyroid program. In our investigation of the order by which the parathyroid-to-thymus cell fate switch occurs, our data suggests that parathyroid cells downregulate the parathyroid program and subsequently upregulate the thymus program.