Differential diagnosis and disease monitoring of Alzheimer's disease dementia (ADD), Parkinson's disease dementia (PDD), and Dementia with Lewy Body (DLB) is crucial since they have specific pathological causes and lesions and consequently require different treatments. At the same time, it is tricky and requires enhanced procedures to extract new valid clinical indexes and biomarkers. Among other biomarkers, resting state eyes-closed electroencephalographic (rsEEG) rhythms have been studied as a possible tool to assess the neurophysiological correlates of dementia. Here, we tested whether rsEEG rhythms would characterize brain arousal in ADD, PDD, and DLB patients. Clinical and rsEEG data of 42 ADD, 42 PDD, 34 DLB, and 40 healthy elderly (Nold) subjects were available in an international archive. Demography, education, and Mini Mental State Evaluation (MMSE) score were matched between the patients’ groups. Individual alpha frequency peak (IAF) determined the delta, theta, alpha1, alpha2, and alpha3 frequency bands. Fixed beta1, beta2, and gamma bands were also considered. Exact low-resolution brain electromagnetic source tomography (eLORETA) estimated the rsEEG cortical sources. Receiver operating characteristic (ROC) curve classified these sources across individuals. DLB patients. Compared to Nold, IAF showed marked slowing in PDD and DLB and moderate in ADD. Furthermore, all patients’ groups showed lower posterior alpha 2 source activities. This effect was dramatic in ADD, marked in DLB, and moderate in PDD. These groups also showed higher occipital delta source activities, but this effect was dramatic in PDD, marked in DLB, and moderate in ADD. The posterior delta and alpha sources allowed good classification accuracies (about 0.85–0.90) between the Nold and diseased individuals and between the ADD and PDD patients. individuals. DLB patients. In quiet wakefulness, delta and alpha sources unveiled different spatial and frequency features of the cortical neural synchronization underpinning brain arousal in ADD, PDD, and DLB patients. Future cross-validation studies will have to test these rsEEG markers for clinical applications and drug discovery.