This study presents a cross-sectional investigation of functional networks in temporal lobe epilepsy (TLE) as they evolve over years of disease. Networks of interest were identified based on a priori hypotheses: the network of seizure propagation ipsilateral to the seizure focus, the same regions contralateral to seizure focus, the cross hemisphere network of the same regions, and a cingulate midline network. Resting functional magnetic resonance imaging data were acquired for 20 min in 12 unilateral TLE patients, and 12 age- and gender-matched healthy controls. Functional changes within and between the four networks as they evolve over years of disease were quantified by standard measures of static functional connectivity and novel measures of dynamic functional connectivity. The results suggest an initial disruption of cross-hemispheric networks and an increase in static functional connectivity in the ipsilateral temporal network accompanying the onset of TLE seizures. As seizures progress over years, the static functional connectivity across the ipsilateral network diminishes, while dynamic functional connectivity measures show the functional independence of this ipsilateral network from the network of midline regions of the cingulate declines. This implies a gradual breakdown of the seizure onset and early propagation network involving the ipsilateral hippocampus and temporal lobe as it becomes more synchronous with the network of regions responsible for secondary generalization of the seizures, a process that may facilitate the spread of seizures across the brain. Ultimately, the significance of this evolution may be realized in relating it to symptoms and treatment outcomes of TLE.