Parkinson's Disease (PD) has been associated with greater total power in canonical frequency bands (i.e., alpha, beta) of the resting electroencephalogram (EEG). However, PD has also been associated with a reduction in the proportion of total power across all frequency bands. This discrepancy may be caused by limited attention to aperiodic activity (1/f) present across all frequency bands. Aperiodic slope has been linked to the ratio of inhibitory to excitatory neural activity, and the aperiodic offset has been linked to the rate of neuronal spiking, both of which are relevant to PD. We examined differences in the resting EEG of PD participants (N = 26) and age-matched controls (CTL; N = 26). We extracted power from canonical frequency bands using traditional methods and also extracted separate parameters for periodic and aperiodic activity. Cluster-based permutation tests over spatial and frequency dimensions indicated that total alpha and beta power during eyes-open and eyes-closed recordings were greater in PD (vs. CTL) participants. Both the slope and the offset of aperiodic activity were greater for PD (vs. CTL) participants. After removing the aperiodic slope and offset, greater alpha power in PD (vs. CTL) was only present in eyes-open recordings and no reliable differences in beta power were observed. Differences between PD and CTLs in the resting EEG are likely driven by aperiodic activity, suggestive of greater relative inhibitory neural activity and greater neuronal spiking. These findings challenge models of PD that emphasise power in canonical frequency bands.