Sleep research has evolved considerably since the first sleep electroencephalography (EEG) 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 are applied to uncover the brain organization and functional connectivity of human sleep with greater spatial resolution. The combination of EEG with different neuroimaging modalities such as Positron Emission Tomography (PET), structural MRI (sMRI) and functional Magnetic Resonance Imaging (fMRI) impose several challenges for sleep studies. For instance, difficulties maintaining and consolidating sleep in an unfamiliar and restricted environment, scanner-related distortions with physiological artifacts may contaminate polysomnography recordings, and the necessity to account for all physiological changes throughout the sleep cycles to better data interpretability. Here, we review the field of sleep neuroimaging in healthy non-sleep-deprived populations, from early findings to more recent developments, discuss the challenges of applying concurrent EEG and imaging techniques to sleep, and possible future directions the field will greatly benefit from.