N-terminal protein α-acetylation (NTA) is a pervasive protein modification that has recently attracted renewed interest. Early studies on NTA were mostly conducted in yeast and metazoans, providing a detailed portrait of the modification, which was indirectly applied to all eukaryotes. However, new findings originating from photosynthetic organisms have expanded our knowledge of this modification, revealing strong similarities as well as idiosyncratic features. Here, we review the most recent advances on NTA and its dedicated machinery in photosynthetic organisms. We discuss the cytosolic and unique plastid NTA machineries and their critical biological roles in development, stress responses, protein translocation and stability. These new findings suggest that the multitasking plastid and cytosolic machineries evolved to support the specific needs of photoautotrophs.