A cutting-edge smart nano-hybrid technology, offering potential benefits for plants, has recently been developed to address the pervasive issue of heavy metal pollution. This study explored the potential of this technology in mitigating chromium (Cr) stress in rapeseed using a nano-based system that integrates 100 mu M hydrogen sulphide (H2S) and 50 mu M manganese nanoparticles (Mn-NPs). This strategy reveals Cr-stress tolerance mechanisms through physiological assessments and transcriptome data analysis. The results demonstrated that Cr stress substantially inhibited rapeseed growth while increasing oxidative damage markers (MDA and ROS levels). Conversely, Mn-NP and H2S co-treatment significantly mitigated these effects, as shown by: (1) restored growth metrics, (2) improved photosynthetic performance and membrane integrity, (3) optimized Mn/H2S homeostasis, and (4) reduced tissue Cr accumulation. The reduction in Cr content was attributed to enhanced Cr-detoxification mechanisms, driven by the upregulation of enzymatic antioxidant activities, like superoxide dismutase, peroxidase, catalase, and ascorbate peroxidase. Transcriptomic profiling revealed marked upregulation of genes involved in core metabolic processes, including photosynthetic pathways, carbon assimilation, secondary metabolite biosynthesis, inositol/phosphatidylinositol signalling systems, and stress-response networks. Under Cr stress, Mn-NP and H2S co-treated rapeseed plants displayed enhanced tolerance, highlighting the crucial role of these signalling agents in activating Cr-defence mechanisms. Our findings demonstrate that the integration of nanotechnology and gasotransmitter signalling molecule H2S presents a novel strategy for enhancing heavy metal tolerance and plant productivity in contaminated soils.