We report on efficient surface-enhanced Raman spectroscopy (SERS) supporting substrates, which are based on deoxyribonucleic acid (DNA)-assisted lithography (DALI) and a layered configuration of materials. In detail, we used nanoscopic DNA origami bowtie templates to form hybrid nanostructures consisting of aligned silver bowtie-shaped particles and apertures of similar shape in a silver film. We hypothesized that this particular geometry could facilitate a four-fold advantage in Raman enhancement compared to common particle-based SERS substrates, and further, we verified these hypotheses experimentally and by finite difference time domain simulations. In summary, our DALI-fabricated hybrid structures suppress the background emission, allow emission predominantly from the areas of high field enhancement, and support additional resonances associated with the nanoscopic apertures. Finally, these nanoapertures also enhance the fields associated with the resonances of the underlying bowtie particles. The versatility and parallel nature of our DNA origami-based nanofabrication scheme and all of the above-mentioned features of the hybrid structures therefore make our optically resonant substrates attractive for various SERS-based applications.