Remediation of arsenic (As) contaminated sites is an urgent necessity for ecological restoration. Pteris vittate (Chinese ladder brake) is a well-known As hyperaccumulator plant that could thrive in As-contaminated sites and accumulate high As concentrations in planta. P. vittata-associated microbiome co-evolved with their host and adapted to elevated As conditions. Therefore, the plant-associated microbial community might play key roles in host survival under elevated As concentrations. While the bacteria community colonizing internal P. vittata tissues, i.e., endophytes, could involve in As biotransformation, their composition and metabolic potentials remain elusive. The objective of the current study was to characterize the root endophytic community and their contribution to As speciation in P. vittata. High AsIII oxidation gene abundance and activity indicate that As biotransformation is more important than other processes. Moreover, members of the core microbiome affiliated with order Rhizobiales drive the AsIII oxidation in P. vittata roots. Besides direct involvement in As metabolism, the Rhizobiales also encoded numerous genomic traits, which could promote P. vittata growth in As-contaminated sites. The current study may be beneficial for future phytoremediation practices.