Adolescent changes in human brain function are not entirely understood. Here we used multi-echo functional magnetic resonance imaging (fMRI) to measure developmental change in functional connectivity (FC) of resting-state oscillations between pairs of 330 cortical regions and 16 subcortical regions in 298 healthy adolescents scanned 520 times. Participants were aged 14-26 years, and were scanned on one to three occasions at least 6 months apart. We found two distinct modes of age-related change in FC: “conservative” and “disruptive”. Conservative development was characteristic of primary cortex, which was strongly connected at 14 years and became even more connected in the period 14-26 years. Disruptive development was characteristic of association cortex and subcortical regions, where connectivity was re-modelled: connections that were weak at 14 years became stronger during adolescence, and connections that were strong at 14 years became weaker. These modes of development were quantified using the maturational index (MI), estimated as Spearman’s correlation between edge-wise baseline FC (at 14 years, FC14) and adolescent change in FC (_FC14−26), at each region. Disruptive systems (with negative MI) were activated by social cognition and autobiographical memory tasks in prior fMRI data, and significantly co-located with prior maps of aerobic glycolysis (AG), AG-related gene expression, post-natal cortical surface expansion, and adolescent shrinkage of cortical thickness. We conclude that human brain organisation is disrupted during adolescence by reorganisation of functional connectivity between association cortical areas, representing metabolically expensive re-modelling of synaptic connectivity in support of the development of social skills and self-awareness during healthy human adolescence.