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Objective: The use of electrical source imaging (ESI) in assessing the source of interictal epileptic discharges (IEDs) is gaining increasing popularity in presurgical work‐up of patients with drug‐resistant focal epilepsy. While vigilance affects the ability to locate IEDs and identify the epileptogenic zone, we know little about its impact on ESI. Methods: We studied overnight high‐density electroencephalography recordings in focal drug‐resistant epilepsy. IEDs were marked visually in each vigilance state, and examined in the sensor and source space. ESIs were calculated and compared between all vigilance states and the clinical ground truth. Two conditions were considered within each vigilance state, an unequalized and an equalized number of IEDs. Results: The number, amplitude, and duration of IEDs were affected by the vigilance state, with N3 sleep presenting the highest number, amplitude, and duration for both conditions (P < 0.001), while signal‐to‐noise ratio only differed in the unequalized condition (P < 0.001). The vigilance state did not affect channel involvement (P > 0.05). ESI maps showed no differences in distance, quality, extent, or maxima distances compared to the clinical ground truth for both conditions (P > 0.05). Only when an absolute reference (wakefulness) was used, the channel involvement (P < 0.05) and ESI source extent (P < 0.01) were impacted during rapid‐eye‐movement (REM) sleep. Clustering of amplitude‐sensitive and ‐insensitive ESI maps pointed to amplitude rather than the spatial profile as the driver (P < 0.05). Interpretation: IED ESI results are stable across vigilance states, including REM sleep, if controlled for amplitude and IED number. ESI is thus stable and invariant to the vigilance state. [ABSTRACT FROM AUTHOR]