The excitability of the sensorimotor (SM1) cortices is reflected in the bilateral ~20 Hz beta oscillations. The extent to which these oscillations subtend the interhemispheric inhibition (IHI) captured by the Transcranial Magnetic Stimulation (TMS) ipsilateral Silent Period (iSP) protocol remains unclear. Therefore, we investigated the relationship between movement-related beta suppression and the iSP, along with their role for manual dexterity. Forty adults underwent an Electroencephalography assessment of beta suppression during volitional left-hand movement and a TMS assessment of iSP recorded from the right hand. In both cases, left SM1 beta oscillations (contralateral to the activated right SM1) were monitored through a proxy signal—the Electromyography of the contracted right hand. Bimanual dexterity was assessed with the Purdue Pegboard. Volitional movement caused significant bilateral SM1 beta suppression in nearly all participants (≥85%). ISPs were observed in every participant. In the proxy signal for the left SM1, the iSP coincided with TMS-evoked high-amplitude beta bursts. These bursts showed significant phase alignment across participants 10–70 ms after the TMS pulse. There was no significant association between the left-/right-hemisphere beta suppression, iSP, and bimanual dexterity. Our results highlight the distinct nature of beta oscillation changes during volitional movement compared with TMS-iSP and show that TMS induces IHI via transcallosal generation of phase-aligned beta bursts. Furthermore, our data suggest that only the initial phase of a beta burst carries an inhibitory effect. It also highlights the possibility of evoking a beta burst with the iSP protocol, opening perspectives for future neuroimaging and modeling studies.