Phyllosphere is a habitat to a variety of viruses, bacteria, fungi, and other microorganisms, which play a fundamental role in maintaining the health of plants and mediating the interaction between plants and ambient environments. A recent addition to this catalogue of microbial diversity was the aerobic anoxygenic phototrophs (AAPs), a group of widespread bacteria that absorb light through bacteriochlorophyll α (BChl a) to produce energy without fixing carbon or producing molecular oxygen. However, culture representatives of AAPs from phyllosphere and their genome information are lacking, limiting our capability to assess their potential ecological roles in this unique niche. In this study, we investigated the presence of AAPs in the phyllosphere of a winter wheat (Triticum aestivum L.) in Denmark by employing bacterial colony based infrared imaging and MALDI-TOF mass spectrometry (MS) techniques. A total of ∼4,480 colonies were screened for the presence of cellular BChl a, resulting in 129 AAP isolates that were further clustered into 21 groups based on MALDI-TOF MS profiling, representatives of which were sequenced using the Illumina NextSeq and Oxford Nanopore MinION platforms. Seventeen draft and four complete genomes of AAPs were assembled belonging in Methylobacterium, Rhizobium, Roseomonas, and a novel Alsobacter. We observed a diverging pattern in the evolutionary rates of photosynthesis genes among the highly homogenous AAP strains of Methylobacterium (Alphaproteobacteria), highlighting an ongoing genomic innovation at the gene cluster level.