Combining atomically resolved DNA-templated silver nanoclusters (AgNCs) with nucleic acid nanotechnology opens new exciting possibilities for engineering bioinorganic nanomaterials with uniquely tunable properties. In this unforeseen cooperation, nucleic acids not only drive the formation of AgNCs but also promote their spatial organization in supra-assemblies. In this work, we confirm the feasibility of this approach using programmable RNA rings to control formation and optical properteis of six individual AgNCs. "Red" (λEXC/λEM = 565/623 nm) and "green" (λEXC/λEM = 440/523 nm) emitting AgNCs are templated on cytosine-rich DNA fragments embedded into the RNA rings. Optical properties of the AgNCs formed on the RNA rings are characterized in detail. While all "red" species passively transition to "green" emitters with time, the initial fluorescent properties and relative stabilities of "red" AgNCs can be regulated by altering the relative orientation of AgNCs within the RNA rings. As such, the oxidative stability increases dramatically for AgNC positioned towards the center of the RNA rings rather than facing outward. Overall, our findings expand the existing AgNC fluorescent toolkit while uncovering the complexity of the AgNC electronic structures with the abundance of possibilities for controlling de-excitation processes.