Plastids evolved from cyanobacteria by endosymbiosis. During the course of evolution, the coding capacity of plastid genomes shrinks due to gene loss or transfer to the nucleus. In the green lineage, however, there were apparent gene gains including that of ycf1. Although its function is still debated, YCF1 has proven to be a useful marker for plastid evolution. YCF1 sequence and predicted structural features unite the plastid genomes of land plants with those of their closest algal relatives, the higher streptophyte algae; YCF1 appears to have undergone pronounced changes during the course of streptophyte algal evolution. Using new data, we show that YCF1 underwent divergent evolution in the common ancestor of higher streptophyte algae and Klebsormidiophycae. This divergence resulted in the origin of an extreme, klebsormidiophycean-specific YCF1 and the higher streptophyte Ste-YCF1. Most importantly, our analysis uncovers a conserved carboxy-terminal sequence stretch within YCF1 that is unique to higher streptophytes and hints at an important, yet unexplored function.