Numerous advances have been made to mitigate the repercussion of toxic metals on photosynthetic prokaryotes, i.e. cyanobacteria. One strategy is exogenous supplementation of plant growth regulators (PGRs). This perhaps intensifies the resistance ability of cyanobacteria to encounter the environmental stresses by augmenting their physiological functioning and decontaminant efficiency. Thus, the aim of the present study was to determine if the PGRs auxin (indole-3 acetic acid, IAA; 300 nM) and cytokinin (kinetin, KN; 10 nM) are able to mitigate the toxic environmentally relevant doses of chromium (CrVI; 100 and 150 µM) in cyanobacteria (Nostoc muscorum ATCC 27,683 and Anabaena sp. PCC 7120). The response was assessed by estimating oxidative stress [in vitro and in vivo (superoxide radical; O2·−, hydrogen peroxide H2O2 and malondialdehyde equivalents contents; MDA)], feasible alteration in whole cell oxygen evolution, ascorbate–glutathione cycle and their metabolites. Intracellular Cr accumulation raised the production of ROS by down-regulating the photosynthetic rate due to decreased pigment contents (Chl a; chlorophyll a, Car; carotenoids and PC; phycocyanin) and reduced growth despite the accelerated activity of the ascorbate–glutathione (AsA-GSH) cycle enzymes (viz. APX; ascorbate peroxidase, GR; glutathione reductase and DHAR; dehydroascorbate reductase). Concurrently, exogenous PGRs (auxin and cytokinin) moderated the negative effects of Cr on the growth, by lowering the cellular Cr accumulation and ROS level and by modulating the pigment system, photosynthesis and a further rise in the efficiency of AsA-GSH cycle, thereby acting as positive regulators of the metal detoxification machinery. Thus, exogenous application of PGRs (auxin and cytokinin) could improve the growth in cyanobacteria in Cr-polluted environments, hence maintaining productivity in paddy cultivation as well as having potential to be used as bio-remediator in metal-contaminated aquatic systems.