The regenerative capacities of an organ rely on the presence of (adult) tissue-specific stem cells. With regards to the thyroid gland, the existence of adult stem cells remains a topic of controversy. Previously, evidence has already suggested the presence of a population of thyroid cells with self-renewal capacity, capable of long-term culturing in vitro. However, the mechanisms that govern these proliferative abilities remain poorly understood. In addition, the slow turnover rate of the tissue-specific cells complicates the search for a distinct marker to identify these cells. Here, we employ a murine label retention assay based on the doxycycline-inducible expression of an H2B-GFP fusion protein which facilitates the observation of these slow cycling cells over time. Induction of the label during embryogenesis followed by a chasing period from birth up to nine months of age allowed for analysis of the GFP label retention at specific time points. Immunofluorescent imaging of the thyroid tissue immediately after birth, and after three, six, and nine months indicated the loss of GFP over time. Moreover, fluorescence-activated cell sorting of the GFP negative (GFP^–) population versus the GFP positive (GFP⁺) population followed by in vitro culturing of the two subgroups into organoids demonstrated a predominant difference in the proliferative capacities of these populations. While GFP⁺ cells were able to form organoids and establish a long-term culture system at all aforementioned time points, this was not the case for the GFP^– subgroup. These data provide the first in-depth examination of thyroid stem/progenitor cell dynamics over time, and suggest the presence of a quiescent thyroid stem cell population which harbours proliferative capacities regardless of age.