Elevated sympathetic vasomotor tone seen in heart failure (HF) may involve dysfunction of the hypothalamic paraventricular nucleus neurons that project to the rostral ventrolateral medulla (PVN‒RVLM neurons). This study aimed to elucidate the role of PVN‒RVLM neurons in the maintenance of resting renal sympathetic nerve activity (RSNA) after myocardial infarction (MI). In male rats, the left coronary artery was chronically ligated to induce MI. The rats received PVN microinjections of an adeno‒associated viral (AAV) vector encoding an archaerhodopsin T (ArchT) with the reporter eYFP. The ArchT rats had abundant distributions of eYFP‒labelled, PVN‒derived axons in the RVLM. In anesthetized ArchT rats with MI (n = 12), optogenetic inhibition of the PVN‒RVLM pathway achieved by 532‒nm‒wavelength laser illumination to the RVLM significantly decreased RSNA. This effect was not found in sham‒operated ArchT rats (n = 6). Other rat groups received RVLM microinjections of a retrograde AAV vector encoding the red light‒drivable halorhodopsin Jaws (Jawsrg) with the reporter GFP, and showed expression of GFP‒labelled cell bodies and dendrites in the PVN. Laser illumination of the PVN at a 635‒nm‒wavelength elicited significant renal sympathoinhibition in Jawsrg rats with MI (n = 9) but not in sham‒operated Jawsrg rats (n = 8). These results indicate that sympathoexcitatory input from PVN‒RVLM neurons is enhanced after MI, suggesting that this monosynaptic pathway is part of the central nervous system circuitry that plays a critical role in generating elevated sympathetic vasomotor tone commonly seen with HF.