Patients with chronic pain disorders such as fibromyalgia (FM) experience a drastic lack of control over the experience of pain. This is arguably one of the main causes for the high distress and impaired quality of life reported by patients. The way perceived control affects subjective pain as well as the underlying neural mechanisms are yet to be investigated. By using functional magnetic resonance imaging (fMRI), we examined the neural correlates of self-controlled compared to computer-controlled heat pain in healthy controls (HC, n=21) and FM patients (n=23). Unlike HC, FM failed to activate brain areas usually involved in pain modulation as well as reappraisal processes (right ventrolateral (VLPFC), dorsolateral prefrontal cortex (DLPFC) and dorsal anterior cingulate cortex (dACC)). In HC, computer-controlled (compared to self-controlled) heat caused significant activations of the orbitofrontal cortex (OFC), whereas FM activated structures typically associated with neural emotion processing (amygdala, parahippocampal gyrus). Additionally, FM displayed significantly decreased gray matter (GM) volumes compared to HC in DLPFC and dACC as well as disrupted functional connectivity (FC) of the VLPFC, DLPFC and dACC with somatosensory and pain (inhibition)-related areas during self-controlled heat stimulation. The functional and structural changes described provide evidence for extensive impairments of pain-modulatory processes in FM. Our investigation represents a first demonstration of dysfunctional neural pain modulation through experienced control in FM according to the extensive functional and structural changes in relevant sensory, limbic and associative brain areas. These areas may be targeted in clinical pain therapeutic treatments involving TMS, neurofeedback or cognitive behavioral trainings.