ABSTRACT Understanding how ageing affects brain function remains a central challenge in neuroscience. Electrophysiological brain imaging techniques provide a near‐direct measure of neuronal activity, which is useful for characterising neurophysiological health. They offer us the ability to track large‐scale networks of functional activity with high temporal precision. The effects of healthy ageing on these networks remain poorly understood, in part due to small sample sizes and limited control for confounding factors in previous studies. Here, we analysed resting‐state source‐reconstructed magnetoencephalography (MEG) data from a large cross‐sectional cohort of healthy adults ( = 612, 18–88 years old) to characterise the effect of age using not only time‐averaged (static), but also transient (dynamic) network activity. We examined time‐averaged power and coherence across canonical frequency bands (, , , , ), as well as transient network dynamics identified using Hidden Markov Modelling. We included many confounding variables known to be affected by age, such as brain volume, as well as head size and position, which have previously been overlooked. Ageing was associated with frequency‐specific changes in oscillatory power, with decreases in low‐frequency (, ) power and increases in high‐frequency () power. Coherence increased across all frequency bands and was positively associated with cognitive performance. Transient network analyses additionally revealed that frontal network occurrences declined with age, with evidence suggesting a compensatory role in supporting cognition. These findings provide a more comprehensive electrophysiological signature for healthy ageing and establish a baseline for detecting pathological change.