Environmental arsenic contamination adversely affects human health, and its accumulation diminishes food quality. Glutathione (GSH) is known to bind and detoxify arsenic and other toxic metals. GSH homeostasis in living cells is maintained via γ-glutamyl cycle. Previously, γ-glutamyl cyclotransferases ( GGCTs) have been shown to be involved in GSH degradation in plants and increasing tolerance to toxic metals. Here we characterized the GGCT2;1 homolog from Camelina sativa for its role in arsenic tolerance and accumulation. Overexpressing CsGGCT2;1 in Camelina resulted in strong tolerance to arsenite (AsIII). Compared to wild-type, overexpression (OE) lines had significantly higher shoot (2.6-3.5-fold) and root (7-10-fold) biomass on AsIII containing media and accumulated 40-60% less arsenic in root and shoot tissues. Further, OE lines had higher chlorophyll content, lower lipid peroxidation and oxidative stress. There was a small but nonsignificant increase in 5-oxoproline (5-OP) in OE lines and the upregulation of Oxoprolinase 1 ( OXP1) suggested accelerated conversion of 5-OP to glutamate, which is then utilized for GSH resynthesis for maintaining homeostasis. Overall, overexpression of GGCT2;1 and it homologs in Camelina and other crops will enable their cultivation on contaminated marginal lands to reduce As accumulation, addressing food safety issues as well as future food and biofuel needs.