Our knowledge about the human resting state is predominantly based on either electroencephalographic (EEG) or functional magnetic resonance imaging (fMRI) methods. While EEG recordings can be performed in seated posture in quiet conditions, the fMRI environment presents a substantial contrast with supine and restricted posture in a narrow tube that is filled with acoustic scanner noise (ASN) at a chainsaw-like volume level. However, the influence of these diverging conditions on resting-state brain activation is neither well studied nor broadly discussed. In order to promote data as a source of sharper hypotheses for future studies, we investigated alterations in EEG-frequency-band power (delta, theta, alpha, beta, gamma) and spatial power distribution as well as cortical vigilance measures in different postures and ASN surroundings over the course of time. Participants (N = 18) underwent three consecutive resting-state EEG recordings with a fixed posture and ASN setting sequence; seated, supine, and supine with ASN (supnoise) using an MRI simulator. The results showed that compared to seated, supnoise, the last instance within the posture sequence, was characterized by lower power and altered spatial power distribution in all assessed frequency bands. This might also have been an effect of time alone. In delta, theta, alpha, and beta, the power of supnoise was also reduced compared to supine, as well as the corresponding distribution maps. The vigilance analysis revealed that in supine and supnoise, the highest and lowest vigilance stages were more dominant compared to the seated and earliest posture condition within the sequence. Hence, our results demonstrate that the differences in recording settings and progress of time are related to changes in cortical arousal and vigilance regulation, findings that should be taken into account more profoundly for hypothesis generation as well as analytic strategies in future resting-state studies.