We conducted a systematic review of the neuroimaging literature examining cognition in old and young adults and quantified these findings in a series of meta-analyses using the activation likelihood estimation technique. In 80 independent samples, we assessed significant convergent and divergent patterns of brain activity across all studies; where task performance was equated or different between age groups; and in four specific cognitive domains (perception, memory encoding, memory retrieval and executive function). Age differences across studies predominantly involved regions within the 'task-positive network' of the brain, a set of interconnected regions engaged during a variety of externally driven cognitive tasks. Old adults engaged prefrontal regions more than young adults. When performance was equivalent, old adults engaged left prefrontal cortex; poorly performing old adults engaged right prefrontal cortex. Young adults engaged occipital regions more than old adults, particularly when performance was unequal and during perceptual tasks. No age-related differences were found in the parietal lobes. We discuss the reliable differences in brain activation with regards to current theories of neurocognitive aging.