Phytoremediation, a cost-effective, eco-friendly alternative to conventional remediation, could expand efforts to remediate arsenic-contaminated soils. As with other pollutants, the plant microbiome may improve phytoremediation outcomes for arsenic-contaminated sites. We used in vitro and in silico methods to compare the arsenic resistance mechanisms, synthesis of extracellular polymeric substances (EPS), biofilm formation, and plant growth-promoting abilities of the endophytes Pseudomonas sp. PD9R and Rahnella laticis PD12R. PD12R, which tolerates arsenate (As(V)) and arsenite (As(III)) to concentrations fivefold greater than PD9R, synthesizes high volumes of EPS in response to arsenic, and sequesters arsenic in the capsular EPS and cells. While arsenic exposure induced EPS synthesis in both strains, only PD12R continued to form biofilms at high As(III) and As(V) concentrations. The effects of endophyte inoculation on Arabidopsis growth varied by strain and As(V) concentration, and PD9R had positive effect on plants exposed to low levels of arsenic. Comparative genomic analyses exploring the EPS synthesis and arsenic resistance mechanisms against other Pseudomonas and Rahnella strains suggest that both strains possess atypical arsenic resistance mechanisms from other plant-associated strains, while the configuration of the EPS synthesis systems appeared to be more broadly distributed among plant-and non-plant-associated strains.