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<i>Pantoea stewartii</i> subsp. <i>indologenes</i> (<i>Psi</i>) is a causative agent of leafspot on foxtail millet and pearl millet; however, novel strains were recently identified that are pathogenic on onions. Our recent host range evaluation study identified two pathovars; <i>P. stewartii</i> subsp. <i>indologenes</i> pv. <i>cepacicola</i> pv. nov. and <i>P. stewartii</i> subsp. <i>indologenes</i> pv. <i>setariae</i> pv. nov. that are pathogenic on onions and millets or on millets only, respectively. In the current study, we developed a pan-genome using the whole genome sequencing of newly identified/classified <i>Psi</i> strains from both pathovars [pv. <i>cepacicola</i> (<i>n</i> = 4) and pv. <i>setariae</i> (<i>n</i> = 13)]. The full spectrum of the pan-genome contained 7030 genes. Among these, 3546 (present in genomes of all 17 strains) were the core genes that were a subset of 3682 soft-core genes (present in ≥16 strains). The accessory genome included 1308 shell genes and 2040 cloud genes (present in ≤2 strains). The pan-genome showed a clear linear progression with >6000 genes, suggesting that the pan-genome of <i>Psi</i> is open. Comparative phylogenetic analysis showed differences in phylogenetic clustering of <i>Pantoea</i> spp. using PAVs/wgMLST approach in comparison with core genome SNPs-based phylogeny. Further, we conducted a horizontal gene transfer (HGT) study using <i>Psi</i> strains from both pathovars along with strains from other <i>Pantoea</i> species, namely, <i>P. stewartii</i> subsp. <i>stewartii</i> LMG 2715^T, <i>P. ananatis</i> LMG 2665^T<i>, P. agglomerans</i> LMG L15, and <i>P. allii</i> LMG 24248^T. A total of 317 HGT events among four <i>Pantoea</i> species were identified with most gene transfer events occurring between <i>Psi</i> pv. <i>cepacicola</i> and <i>Psi</i> pv. <i>setariae</i>. Pan-GWAS analysis predicted a total of 154 genes, including seven gene-clusters, which were associated with the pathogenicity phenotype (necrosis on seedling) on onions. One of the gene-clusters contained 11 genes with known functions and was found to be chromosomally located.