Members of the Ralstonia solanacearum species complex (RSSC) are naturally competent soil-borne vascular pathogens that causes severe outbreaks in staple carbohydrate and high-value crops like banana (Musa spp.), potato (Solanum tuberosum), and tomato (S. lycopersicum). Phylotypes I and II have been documented in Martinique since the 1960s, however in 1999 a novel lineage was identified, prompting a large-scale sampling effort. This new lineage, referred to as 4NPB, can infect cucurbits and Heliconia spp. and is more aggressive on solanaceous crops than previous variants. We sequenced 487 RSSC isolates sampled across Martinique and French Guiana during the emergence of this novel lineage. Pangenome and phylogenetic analyses were performed to identify genomic changes linked with the emergence of the new lineage. This analysis reveals the 4NPB population likely emerged from an ancestral mainland population infecting Musa sp. The emergence of the 4NPB lineage is associated with the exchange of Type 3 secreted effectors and multiple genes with predicted catalytic activity. Recombination hotspots found between 4NPB and close relatives include various two partner secretion systems potentially involved in intra-species competition and signaling. These changes may underlie the altered pathogenicity and host-range profile of 4NPB, contributing to the dramatic expansion of this lineage across Martinique.