SummaryPlant mitochondrial transcripts undergo maturation processes at both termini. Although frequently observed, the post‐transcriptional formation of mature 5′ ends is still poorly understood. We now analyzed the processing of transcripts derived from the mitochondrial ccmC gene, coding for a component of the cytochrome c maturation system. In Arabidopsis thaliana (Arabidopsis) there are two mitochondrial ccmC configurations, discriminated by a 66‐bp sequence segment located approximately 500 bp upstream of the ccmC gene. In Arabidopsis accessions these divergent mitochondrial genotypes correlate with the generation of two different 5′ termini that map to positions around −484 in accession Columbia (Col ccmC genotype) or −390 in accession C24 relative to the translation start codon (C24 ccmC genotype). Previously we identified RNA PROCESSING FACTOR 3 (RPF3), a pentatricopeptide repeat (PPR) protein required for the maturation of ccmCmRNAs with −484 5′ ends transcribed from the Col ccmC genotype. Now we identified several accessions defective in maturation of ccmC transcripts. Taking advantage of this natural genetic variation we identified RNA PROCESSING FACTOR 6 (RPF6), a PPR protein necessary for the generation of ccmCmRNAs with −390 5′ ends transcribed from the C24 ccmC genotype. Both Col‐type and C24‐type accessions encode RPF3 and RPF6 so that they can process ccmC transcripts derived from the two different mitochondrial genotypes. These factors and their cognate RNA recognition sites in the different ccmC genotypes are an intriguing example for the evolution of two co‐adapted cyto‐nuclear systems required for the same process i.e. 5′ maturation of ccmC transcripts.