BACKGROUND: Depression is a prevalent and debilitating affective disorder characterized by the dominance and persistence of depressive rumination. Mindfulness-based cognitive therapy (MBCT) is an effective treatment for recurrent depression developed specifically to target rumination and recurrence risk by training metacognitive awareness and adaptive attention, emotion, and self-regulation skills. However, the underlying mechanisms by which mindfulness training impacts maladaptive depressive rumination are not well understood, and a deeper understanding of its effects on the complex brain dynamics during depressive rumination is needed. METHODS: In a randomized controlled functional magnetic resonance imaging (fMRI) study (N = 80), we examined dynamic neural changes during resting-state fMRI of an experimentally induced rumination state before and after treatment with MBCT (n = 27) for recurrent depression in addition to treatment as usual (TAU) or TAU alone (n = 21). More specifically, we characterized the changes during a depressive rumination state as a repertoire of metastable substates, each with an occurrence frequency (fractional occupancy) and stability (lifetimes). RESULTS: We found that MBCT training compared with TAU altered the fractional occupancy of a salience-somatomotor metastable substate during the depressive rumination state. These dynamic network changes in turn were associated with reduced trait rumination posttreatment and reduced depressive symptoms at the 3-month follow-up. CONCLUSIONS: In a ruminative state, changes in the dynamics of the somatosensory-salience network following mindfulness training was associated with improved clinical outcomes and reduced trait rumination, which may provide insight into candidate brain mechanisms or markers of treatment response to MBCT.