Plant parasitic root-knot nematodes (RKN) such as Meloidogyne incognita cause significant crop losses worldwide. Although RKN are polyphagous, with wide host ranges, races with differing host compatibilities have evolved. Associations between genotype and infection phenotype in M. incognita have not yet been discovered. In this study, 48 M. incognita isolates were collected from geographically diverse fields in Japan and their genomes sequenced. The isolates exhibited various infection compatibilities to five sweetpotato (SP) cultivars and were assigned to SP races. Genome-wide association analysis identified 743 SNPs affecting gene coding sequences, a large number of which (575) were located on a single 1 Mb region. To examine how this polymorphic region evolved, nucleotide diversity (Pi) was scanned at the whole genome scale. The SNP-rich 1 Mb region exhibited high Pi values and was clearly associated with the SP races. SP1 and 2 races showed high Pi values in this region whereas the Pi values of SP3, 4, and 6 were low. Principal component analysis of isolates from this study and globally collected isolates showed selective divergence in this 1 Mb region. Our results suggest for the first time that the host could be a key determining factor stimulating the genomic divergence of M. incognita.