The robust coevolution of catalytically active, metabolically cooperating prebiotic RNA replicators were investigated using an RNA World model of the origin of life based on physically and chemically plausible first principles. The Metabolically Coupled Replicator System assumes RNA replicators to supply metabolically essential catalytic activities indispensable to produce nucleotide monomers for their own template replication. Using external chemicals as the resource and the necessary ribozyme activities, Watson-Crick type replication produces complementary strands burdened by high-rate point mutations (insertions, deletions, substitutions). Metabolic ribozyme activities, replicabilities and decay rates are assigned to certain sequence and/or folding (thermodynamical) properties of single-stranded RNA molecules. Short and loosely folded sequences are given replication advantage, longer and tightly folded ones are better metabolic ribozymes and more resistant to hydrolytic decay. We show that the surface-bound MCRS evolves stable and metabolically functional communities of replicators of almost equal lengths, replicabilities and ribozyme activities. Being highly resistant to the invasion of parasitic (non-functional) replicators, it is also stable in the evolutionary sense. The template replication mechanism selects for catalytic “promiscuity”: the two (complementary) strands of the same evolved replicator will often carry more than a single catalytically active motif, thus maximizing functionality in a minimum of genetic information.