•Developmental stuttering (DS) relies on dysfunctional neural exchange: the supplementary motor area (SMA) may play a key role.•We used combined TMS/EEG to investigate functional connectivity of the SMA “complex” in DS.•Abnormal neural timing in DS is inferred which helps to understand the pathophysiology of DS and develop new treatments. Brain dynamics in developmental stuttering (DS) are not well understood. The supplementary motor area (SMA) plays a crucial role, since it communicates with regions related to planning/execution of movements, and with sub-cortical regions involved in paced/voluntary acts (such as speech). We used TMS combined with EEG to shed light on connections in DS, stimulating the SMA. TMS/EEG was recorded in adult DS and fluent speakers (FS), stimulating the SMA during rest. TMS-evoked potentials and source distribution were evaluated. Compared to FS, stutterers showed lower activity of neural sources in early time windows: 66–82 ms in SMA, and 91–102 ms in the left inferior frontal cortex and left inferior parietal lobule. Stutterers, however, showed higher activations in later time windows (i.e. from 260–460 ms), in temporal/premotor regions of the right hemisphere. These findings represent the functional counterpart to known white matter and cortico-basal-thalamo-cortical abnormalities in DS. They also explain how white matter abnormalities and cortico-basal-thalamo-cortical dysfunctions may be associated in DS. Finally, a mechanism is proposed in which compensatory activity of the non-dominant (right) hemisphere is recruited. DS may be a disorder of neural timing that appears to be delayed compared to FS; new mechanisms that support stuttering symptoms are inferred; the SMA may be a promising target for neuro-rehabilitation.