Genetic recoding, a process that modifies genome templated protein sequence, plays an important role especially in the small genomes of viruses and bacteria. Chloroplasts have evolved from cyanobacterial ancestry and mainly retain the prokaryotic gene expression machinery. I-iota, a plastome mutant of Oenothera (the evening primrose), carries a single adenine insertion in a polyA stretch near to the 5’-end of the atpB gene, encoding the β-CF1 subunit of the ATP synthase This causes formation of a truncated protein. Surprisingly, a full-length AtpB protein is detectable in I-iota leaves, suggesting the presence of genetic recoding operating in I-iota. In order to analyze this phenomenon in more detail, several tobacco transplastomic lines were generated inducing and destroying genetic recoding of atpB. We identified that a two adenine (+2A) insertion was more efficiently compensated in plants than +1A, -1A or -2A mutations at the same location. Furthermore, a homopolymeric composition of the polyA stretch is essential for successful recoding: plants carrying a destroyed polyA stretch have an albino-phenotype, indicating the absence of genetic recoding. Here we show evidence for genetic recoding acting in the chloroplast that plays presumablya compensatory function and enables correction of indels in an essential gene for autotrophic growth.