Meditation practice is suggested to engage training of cognitive control systems in the brain. To evaluate the functional involvement of attentional and cognitive monitoring processes during meditation, the present study analysed the electroencephalographic synchronization of fronto-parietal (FP) and medial-frontal (MF) brain networks in highly experienced meditators during different meditation states (focused attention, open monitoring and loving kindness meditation). The aim was to assess whether and how the connectivity patterns of FP and MF networks are modulated by meditation style and expertise. Compared to novice meditators, (1) highly experienced meditators exhibited a strong theta synchronization of both FP and MF networks in left parietal regions in all mediation styles, and (2) only the connectivity of lateralized beta MF networks differentiated meditation styles. The connectivity of intra-hemispheric theta FP networks depended non-linearly on meditation expertise, with opposite expertise-dependent patterns found in the left and the right hemisphere. In contrast, inter-hemispheric FP connectivity in faster frequency bands (fast alpha and beta) increased linearly as a function of expertise. The results confirm that executive control systems play a major role in maintaining states of meditation. The distinctive lateralized involvement of FP and MF networks appears to represent a major functional mechanism that supports both generic and style-specific meditation states. The observed expertise-dependent effects suggest that functional plasticity within executive control networks may underpin the emergence of unique meditation states in expert meditators.