By definition, hallucinations occur only in the full waking state. Yet similarities to sleep-related experiences such as hypnagogic and hypnopompic hallucinations, dreams and parasomnias, have been noted since antiquity. These observations have prompted researchers to suggest a common aetiology for these phenomena based on the neurobiology of rapid eye movement (REM) sleep. With our recent understanding of hallucinations in different population groups and at the neurobiological, cognitive and interpersonal levels, it is now possible to draw comparisons between the 2 sets of experiences as never before. In the current article, we make detailed comparisons between sleep-related experiences and hallucinations in Parkinson’s disease, schizophrenia and eye disease, at the levels of phenomenology (content, sensory modalities involved, perceptual attributes) and of brain function (brain activations, resting-state networks, neurotransmitter action). Findings show that sleep-related experiences share considerable overlap with hallucinations at the level of subjective descriptions and underlying brain mechanisms. Key differences remain however: (1) Sleep-related perceptions are immersive and largely cut off from reality, whereas hallucinations are discrete and overlaid on veridical perceptions; and (2) Sleep-related perceptions involve only a subset of neural networks implicated in hallucinations, reflecting perceptual signals processed in a functionally and cognitively closed-loop circuit. In summary, both phenomena are non-veridical perceptions that share some phenomenological and neural similarities, but insufficient evidence exists to fully support the notion that the majority of hallucinations depend on REM processes or REM intrusions into waking consciousness.