Our results here demonstrate the possibility of assembling prebiotic peptidyl-RNA via strand replacement and transfer from (N-formyl)-aminoacyl mixed anhydrides. We note dipeptides have been shown to have sequence specific activities relevant to the origins of life, such as vesicle growth. Stable duplex and strand replacement are the prerequisites for peptidyl assembly. Here, the peptide directly forms at the CCA-ending overhang, as in extant tRNA. The hydrolytic stability of formyl-dipeptidyl-RNA varies with amino acid sequence. Our investigations into the mechanism of N-formylamino acid transfer suggest that 5-(4H)-oxazolones are not implicated in the mechanism of transfer. The transfer of N-acylamino acids onto 2',3'-diol termini in a nicked-duplex or a nicked-loop, and onto aminoacyl esters in nicked loops show no stereoselectivity. Due to the similarity in chemistry, it is conceivable that a transition from trimer-mixed anhydride donors to adenylate-mixed anhydrides which we see in modern biology is simpler than those template chemistries presented previously. Our results also highlight the difficulty of avoiding peptidyl-transfer in systems capable of transferring aminoacyl residues from free amino acid:phosphate mixed anhydrides to 2',3'-diol termini of RNA.