During postembryonic development, a larval skeletal muscle motoneuron, MN-1 in abdominal segments 7 and 8, becomes respecified to innervate the terminal cardiac chamber of adult Manduca sexta. Neural tracing techniques and electrophysiology were used in this study to describe the anatomical and physiological remodeling of this identified motoneuron. During metamorphosis the MN-1 in segments 7 and 8 undergoes dendritic reorganization. Long new dendrites extend anteriorly in the terminal ganglion neuropil. Intracellular and extracellular recordings showed that broader action potentials, increased firing rate, and development of a bursting activity pattern accompany MN-1 respecification. Cardiac mechanograms showed that MN-1 activity bursts always correlate with the anterograde cardiac beat. Bilateral MNs-1 fire at similar times to activate and sustain the putative cardiac pacemaker activity of the terminal chamber synergistically. After remodeling, MN-1 output could be influenced rapidly by sensory inputs during evoked cardiac reversal. The effect is exerted by inhibition of MN-1 firing that, in turn, causes early blockade of the anterograde beat and reversal to the retrograde direction of beat.