Previous studies regarding developmental stuttering (DS) suggest that motor neural networks are strongly affected. Transcranial magnetic stimulation (TMS) was used to investigate neural activation of the primary motor cortex in DS during movement execution, and the influence of muscle representations involved in movements on “surrounding” ones. TMS was applied over the contralateral abductor digiti minimi (ADM) motor representation, at rest and during the movement of homologue first dorsal interosseous muscles (tonic contraction, phasic movements cued by acoustic signalling, and “self-paced” movements). Results highlighted a lower cortico-spinal excitability of ADM in the left hemisphere of stutterers, and an enhanced intracortical inhibition in their right motor cortex (in comparison to fluent speakers). Abnormal intracortical functioning was especially evident during phasic contractions cued by “external” acoustic signals. An exaggerated inhibition of muscles not directly involved in intended movements, in stuttering, may be useful to obtain more efficient motor control. This was stronger during contractions cued by “external” signals, highlighting mechanisms likely used by stutterers during fluency-evoking conditions.