Genome dynamics is crucial for bacterial genome evolution and adaptation. Here we reveal the unexpectedly fast genome diversification occurring within a highly genetically cohesive population of soil bacteria Streptomyces. We applied a reverse ecology sampling strategy in order to isolate sympatric Streptomyces that have diverged within a short evolutionary time. For this purpose, we isolated bacteria from rhizospheric soil aggregates in the range of mm3 size and distant at the centimeter scale. We selected isolates that shared 100% of identity in 16S rRNA sequences and presented a high degree of similarity in MLST and ANI genome comparisons. We concluded that the isolated strains were all highly related at the intra-specific level and according to the sampling scheme should derive from a common ancestor over a very short evolutionary time. By comparing the genome sequences of 18 isolates (genome size ca. 11.7 Mb), we identified at least 25 genomic islands (>10 kb) scattered along the chromosome, but with a higher frequency in the terminal regions of the linear chromosome, including in some cases the chromosomal end. Some of them exhibit clear signatures of integrated and conjugative elements, while some other include secondary metabolite biosynthetic genes. In addition, some isolates also diverge by the presence of large plasmids (100 to 400 kb). Different patterns of inhibitory capacities were distinguished within the population. Hence, while only some Streptomyces isolates exhibited inhibitory activities against other bacterial coinhabitants (e.g. Bacillus), all the Streptomyces strains could develop together. This suggests that inhibitory activities provided by some isolates may constitute ‘public goods’ to the Streptomyces community, and this by the mean of differentiation of the secondary metabolism gene repertoire. As a proof of concept that rapid genome dynamics impacts population ecology, we inactivated a biosynthetic gene cluster gene (i.e. NRPS) specific of one inhibitory strain and observed the abolition of the inhibitory activity. Together our data support the hypothesis that the high level of evolvability of the Streptomyces genome impacts structuring and adaptation of natural bacterial communities.