Horizontal gene transfer is a major force driving evolution in prokaryotes and has played a direct role in the evolution of pathogenicity and virulence in numerous bacterial pathogens. We have identified a large family of 'integrative and conjugative elements' widely distributed among plant-associated Pseudomonas spp. (PsICEs), including P. syringae. While PsICEs had diverged at the nucleotide level, they shared the same integration site and a conserved syntenic set of backbone genes interspersed with various accessory regions. Accessory regions included genes for resistance to heavy metals, type 3 secretion system effectors but the most common element is the transposon Tn6212. The kiwifruit pathogen P. syringae pv. actinidiae (Psa) was responsible for a devastating agricultural pandemic in 2008. Sequencing of globally dispersed isolates revealed three divergent PsICEs lineages carrying Tn6212 were independently acquired by Psa pandemic strains, suggesting this transposon might confer a selective advantage to its host. Tn6212 provided a competitive advantage to Psa NZ13 when grown in succinate, malate, fumarate and citrate as only carbon sources. RNA-seq experiments demonstrated Tn6212 can manipulate expression of both core-chromosomal and PsICE genes. In Psa, the PsICEs were also responsible for the acquisition of resistance to copper, the most common antimicrobial compound used in agriculture. Interestingly, while copper resistance provided a selective advantage, the acquisition of the new element did not impose any competitive fitness cost to Psa NZ45. We have described a novel family of ICEs and showed how their accessory genes can contribute to the fitness of Psa. PsICEs, having control over both vertical and horizontal modes of transmission, minimizing costs for host cell while introducing new beneficial traits, are potent vehicles of microbial evolution.