This exploratory study tested the hypothesis that Huntington’s disease (HD) is characterized by distinct abnormalities in resting-state electroencephalographic (rsEEG) rhythms compared to Alzheimer’s disease (AD). Clinical and rsEEG data were collected from 35 patients with HD, 81 patients with AD, and 102 healthy controls (HC). The rsEEG cortical source activations from 30 electrodes were estimated using eLORETA and were harmonized across clinical sites. Compared to the HC group, both the HD and AD groups showed widespread increases in rsEEG delta source activation and decreases in alpha source activation, with the HD patients exhibiting the most pronounced frontal effects. In patients with HD, those abnormal rsEEG source activations were associated with cognitive, motor, and functional deficits. Patients with HD were characterized by a particular slowing of frontal rsEEG rhythms associated with clinically relevant variables. A topographically widespread slowing of cortical oscillatory activity was observed in both HD and AD groups, with a particularly pronounced frontal effect in HD, which may predict a greater impact on the sleep–wake cycle. These observations should be considered exploratory and need validation in future studies with enhanced vigilance monitoring during longer rsEEG recordings.