Research has shown that many copy number variations (CNVs) increase the risk of neurodevelopmental disorders (e.g., autism, ADHD, schizophrenia). However, little is known about the effects of CNVs on brain development and function. Resting-state electroencephalography (EEG) is a suitable method to study the disturbances of neuronal functioning in CNVs. We aimed to determine whether there are resting-state EEG signatures that are characteristic of children with pathogenic CNVs. EEG resting-state brain activity of 109 CNVs carriers (66 deletion carriers, 43 duplication carriers) aged 3 to 17 years was recorded for 4 minutes. To better account for developmental variations, EEG indices (power spectral density and functional connectivity) were corrected with a normative model estimated from 256 Healthy Brain Network controls. Results showed increased beta and gamma power in posterior regions as well as global under-connectivity in several frequency bands in CNVs carriers. Deletion and duplication carriers can be differentiated by their connectivity in low alpha frequencies: duplication carriers connectivity was more disrupted than deletion carriers. The distinctive connectivity perturbations were found to be most prominent during adolescence. The results suggest that CNVs carriers show electrophysiological alterations compared to neurotypical controls, regardless of the gene dosage effect and of their affected genomic region. Moreover, a specific signature of the brain alterations associated with duplications was found.