Population genetic analyses based on genome-wide sequencing data have been carried out for Sinorhizobium medicae and S. meliloti, two closely related bacterial species forming nitrogen-fixing symbioses with plants of the genus Medicago. However, genome coverage was low or the isolates had a broad geographic distribution, making it difficult to interpret the estimated diversity and to unravel the early events underlying population genetic variations and ecological differentiation.Here, to gain insight into the early genome level variation and diversification within S. meliloti populations, we first used Illumina paired-end reads technology to sequence a new clone of S. meliloti strain GR4, a highly competitive strain for alfalfa nodulation. The Illumina data and the GR4 genome sequence previously obtained with 454 technology were used to generate a high-quality reference genome sequence. We then used Illumina technology to sequence the genomes of 13 S. meliloti isolates representative of the genomic variation within the GR4-type population, obtained from a single field site with a high degree of coverage. The genome sequences obtained were analyzed to determine nucleotide diversity, divergence times, polymorphism and genomic variation. Similar low levels of nucleotide diversity were observed for the chromosome, pSymB and pSymA replicons. The isolates displayed other types of variation, such as indels, recombination events, genomic island excision and the transposition of mobile elements.Our results suggest that the GR4-type population has experienced a process of demographic expansion and behaves as a stable genotypic cluster of genome-wide similarity, with most of the genome following a clonal pattern of evolution. Although some of genetic variation detected within the GR4-type population is probably due to genetic drift, others might be important in diversification and environmental adaptation.