Sleep research has evolved considerably since the first sleep electroencephalography recordings in the 1930s and the discovery of well-distinguishable sleep stages in the 1950s. While electrophysiological recordings have been used to describe the sleeping brain in much detail, since the 1990s neuroimaging techniques have been applied to uncover the brain organization and functional connectivity of human sleep with greater spatial resolution. The combination of electroencephalography with different neuroimaging modalities such as positron emission tomography, structural magnetic resonance imaging and functional magnetic resonance imaging imposes several challenges for sleep studies, for instance, the need to combine polysomnographic recordings to assess sleep stages accurately, difficulties maintaining and consolidating sleep in an unfamiliar and restricted environment, scanner-induced distortions with physiological artefacts that may contaminate polysomnography recordings, and the necessity to account for all physiological changes throughout the sleep cycles to ensure better data interpretability. Here, we review the field of sleep neuroimaging in healthy non-sleep-deprived populations, from early findings to more recent developments. Additionally, we discuss the challenges of applying concurrent electroencephalography and imaging techniques to sleep, which consequently have impacted the sample size and generalizability of studies, and possible future directions for the field.