Spontaneous brain activity, as observed in functional neuroimaging, has been shown to display reproducible structure that expresses brain architecture and carries markers of brain pathologies. An important view of modern neuroscience is that such large-scale structure of coherent activity reflects modularity properties of brain connectivity graphs. However, to date, there has been no demonstration that the limited and noisy data available in spontaneous activity observations could be used to learn full-brain probabilistic models that generalize to new data. Learning such models entails two main challenges: i) modeling full brain connectivity is a difficult estimation problem that faces the curse of dimensionality and ii) variability between subjects, coupled with the variability of functional signals between experimental runs, makes the use of multiple datasets challenging. We describe subject-level brain functional connectivity structure as a multivariate Gaussian process and introduce a new strategy to estimate it from group data, by imposing a common structure on the graphical model in the population. We show that individual models learned from functional Magnetic Resonance Imaging (fMRI) data using this population prior generalize better to unseen data than models based on alternative regularization schemes. To our knowledge, this is the first report of a cross-validated model of spontaneous brain activity. Finally, we use the estimated graphical model to explore the large-scale characteristics of functional architecture and show for the first time that known cognitive networks appear as the integrated communities of functional connectivity graph.