Thyroid hormone (TH) dysregulation is one of the most prevalent endocrine defects worldwide (3.8% of EU citizens). Regulation of TH output from the thyroid is dependent on secretion of thyroid-stimulating-hormone (TSH) from a small population of pituitary thyrotrophs in response to hypothalamic thyrotropin-releasing-hormone (TRH) and thyroid hormone feedback. Importantly, diagnosis of hypothyroidism is based on a single TSH measurement, thus dismissing the pulsatile property of TSH secretion and the non-linear TSH-TH relationship upon disease onset and subsequent recovery. Despite the undeniable implication of thyrotropes in the hypothalamus-pituitary-thyroid (HPT) axis regulation, little is known about the mechanisms underlying pulsatile and adaptive TSH secretion. The aim of this study is to decipher how thyrotropes form a very finely regulated and highly plastic functionally-organised cell population capable of adapting to TH demand. Pituitary-scale 3D imaging revealed an anatomical thyrotroph network that is established during late embryogenesis, when TSHß-positive cells begin forming homotypic anatomical network motifs, prior to an increase in TH demand during the neonate period. We found that, at weaning, concomitantly with a decrease in TH levels, TSH-expressing thyrotroph motifs disaggregate. Lineage-tracing experiments unveiled that thyrotroph cluster motifs persist after weaning in the form of intermingled thyrotroph sub-sets: a sub-population of TSHß-expressing (TSHhigh) thyrotrophs and another subset of thyrotrophs that express low, if any, TSHß hormone subunit (TSHlow). Using in vivo calcium imaging in both freely-moving and anesthetized TSHβ-crexR26fl-flGCaMP6f mice, we show that the surprisingly unified cell ensemble of TSHhigh and TSHlow thyrotrophs generates large-scale intercellular waves of the universal second messenger Ca2+, which recur autonomously and independently of hypothalamic TRH inputs. This mode of intercellular communication is a network signature of this composite thyrotroph population, which persists in a mouse model of thyroid dysfunction, since the thyrotroph network-driven wave generator of Ca2+ oscillations is robust regardless of the significant increase in TSH cell mass upon hypothyroidism onset. Altogether, our findings redefine the role of pituitary thyrotrophs in HPT axis function. Their division into two sub-populations of cells organised as a single network may explain TSH pulsatility and the non-linear TSH-TH relationship. This shall provide a clearer understanding of the interactions between the pituitary thyrotrophs and the thyroid gland, thus allowing a refinement of current diagnosis and treatment of thyroid hormone defects.