The noradrenergic locus coeruleus (LC) is a fundamental component in the regulation of brain states supporting wakefulness. However, the possibility that it also plays a role for sleep has been around for many years. Gaining a more profound understanding of LC activity in the sleeping brain is crucial for better comprehension of sleep progression in health and disease. Using fiber photometry recordings combined with polysomnography, we show that NREMS alternates between two distinct brain states that arise from infraslow (~50s) activity fluctuations in LC neurons. During NREMS, high LC transient activity prevented REMS transitions and led to two types of brain rhythm and autonomic signatures. Transients with higher amplitude were accompanied by microarousals and coincided with cortical, thalamic, and cardiac activation. Conversely, transients with a lower amplitude were associated with thalamic and cardiac activation but rather cortical deactivation in the absence of EMG signal. Moreover, low LC activity levels served as windows of opportunity for transitions to REMS throughout which LC’s activity remained at minimal levels. The LC-induced brain state alternation regulated natural cycle length but also contributed to imposing a lower limit on NREMS-REMS cycle duration, as demonstrated by natural cycle shortening through a minimal (~50s) inter-REMS-interval during REMS restriction. Furthermore, exposing the animals to a stress-inducing waking state elevated LC activity levels during subsequent NREMS causing increased arousability and delayed REMS onset. In summary, we identify a novel brain-state-induced architectural unit of the undisturbed mammalian NREM-REMS cycle that can lead to sleep disruptions after adverse wake experience