The remarkable ability of the bacteriophages to adapt to the variable ecological situations is undoubtedly one of the key features of these viruses lifestyle. It is widely believed that the main mechanism of this adaptation relies on short-term (co)evolution processes. Phage evolution has been extensively studied using the model laboratory microcosms. A large body of information also comes from the comparison of the phage isolates and/or phage genomes of unknown or random origin. Here we use in-depth genomic and experimental comparative analysis of the series of highly related and ecologically linked coliphage isolates. We studied a set of the N4-like G7C-related podoviruses isolated in 2006-2013 from the horse faeces sampled from a single animal population. Our data indicate that in contrast to the in vitro co-evolving phage G7C – E.coli 4s system, where the evolutionary adaptations were driven predominantly by point mutations, the impact of the genetic exchange of the phage(s) with the available genetic pool of the community plays a very significant role in shaping of the viral genomes in an open and complex natural microbial community. We detected several types of the modular exchange events, including homing nucleases mobility, mobile type I introns invasions, swapping of the fragments of the receptor recognition proteins and else. The interpretation of these observations is based on the extensive experimental study of G7C phage biology encompassing the detailed adsorption apparatus characterization including RBPs X-ray crystallography, virion Cryo-EM reconstruction and biochemical analysis of the enzymatic activity of the tailspikes, the intron activity confirmation and else. Our conclusions are in agreement with the results of analysis of the set of T5-like isolates obtained from the same location. So one can conclude that the evolutionary trajectories of phage genomes are determined not only by the environmental conditions but also by the composition of the local community metagenome.