Plasmonic nanocavities are highly desirable for optical sensing because of their singular ability to confine light into deep subwavelength volumes. Yet, it remains profoundly challenging to fabricate structurally resilient nanocavities with high fidelity, and to obtain direct, noninvasive visualization of the plasmonic hotspots within such constructs. Herein, highly precise and robust nanocavities, entitled DNA‐silicified template for Raman optical beacon (DNA‐STROBE), are engineered by using silicified DNA scaffolds for spatial organization of discrete plasmonic nanoparticles. In addition to substantially enhancing structural stability and chemical inertness, DNA silicification significantly improves nanogap control, resulting simultaneously in large and controlled local electromagnetic field enhancement. The ultrasmall mode volume of the DNA‐STROBE constructs promotes single‐molecule occupancy enabling surface‐enhanced Raman spectroscopy (SERS) observations of single‐molecule activity even at elevated background concentration, significantly relaxing the restrictive pico‐ to nanomolar molecular concentration condition typically required for such investigations. Additionally, leveraging super‐resolution SERS measurements allows noninvasive and diffraction‐unlimited spatial profiling of otherwise unresolvable plasmonic hotspots. The highly programmable and reproducible nature of the DNA‐STROBE, coupled with its quantitative label‐free molecular readouts, provides a versatile platform with applications across the spectrum of nanophotonics and biomedical sciences.