The corticotropin-releasing hormone (CRH) is a peptide associated with stress and anxiety that acts as a potent modulator in the central nervous system. The thalamic reticular nucleus (TRN) displays high expression of the CRH receptor 1 (CRHR1), but whether CRH modulates key TRN functions, such as sleep spindle rhythmogenesis, has not yet been explored.Using viral mapping, we identified diverse extra-hypothalamic CRH afferents to the TRN, such as the basolateral amygdala, zona incerta and subnuclei within the geniculate nucleus. Combining polysomnographic and photometric recordings in mice, we found that CRH release at the TRN during non-rapid-eye movement sleep (NREMS) exhibits an infra-slow oscillatory pattern (~50s period) and that CRH levels anticorrelate with oscillations of EEG sigma power, a proxy for sleep spindles. Photoactivating CRH release during NREMS decreased sigma power and sleep stability, as indicated by the higher density of microarousals. Photoinhibiting CRH release, instead, consolidated NREMS by increasing delta power and reducing the occurrence of microarousals. Finally, ex-vivo patch-clamp recordings showed that CRHR1 activation decreases TRN neurons’ propensity to fire low-threshold calcium bursts. Thus, CRH impacts NREMS stability by affecting the cellular substrates of sleep spindle rhythmogenesis, providing a potential target to normalize sleep impairments associated with stress and anxiety.