Author Summary The brain is spontaneously active even in the absence of specific sensations or movements. This ongoing activity arises from the interactions among hundreds of thousands of neurons, which has been captured by a variety of distinct functional networks predictive of healthy and pathological brain functions. The global dynamical states and overarching network principles that underlie such ongoing brain activity are not well understood. Here we identify avalanche dynamics and “friendship” networks as two major features of ongoing activity in the frontal cortex of nonhuman primates. We demonstrate their stability over weeks in the face of local network changes. Deviation from avalanche dynamics and “friendship” organization might provide robust biomarkers to identify normal and pathological brain states. Abstract Ongoing neuronal activity in the brain establishes functional networks that reflect normal and pathological brain function. Most estimates of these functional networks suffer from low spatiotemporal resolution and indirect measures of neuronal population activity, limiting the accuracy and reliability in their reconstruction over time. Here, we studied the stability of neuronal avalanche dynamics and corresponding reconstructed functional networks in the adult brain. Using chronically implanted high-density microelectrode arrays, the local field potential (LFP) of resting-state activity was recorded in prefrontal and premotor cortex of awake nonhuman primates. Avalanche dynamics revealed stable scaling exhibiting an inverted parabolic profile and collapse exponent of 2 in line with a critical branching process over many days and weeks. Functional networks were based on a Bayesian-derived estimator and demonstrated stable integrative properties characterized by nontrivial high neighborhood overlap between strongly connected nodes and robustness to weak-link pruning. Entropy-based mixing analysis revealed significant changes in strong link weights over weeks. The long-term stability in avalanche scaling and integrative network organization in the face of individual link weight changes should support the development of noninvasive biomarkers to characterize normal and abnormal brain states in the adult brain.