The application of elicitors is regarded as one of the most efficient strategies for augmenting secondary metabolite contents in medicinal plants. There are numerous reports documenting the impact of methyl jasmonate (meJA) on plant growth and biosynthesis of secondary metabolites. However, the underlying physiological response of the plants towards meJA elicitation is understudied. Thus, the current study focused on evaluating the influence of meJA on growth performance, reactive oxygen species (ROS)/antioxidants crosstalk, and expression of bioactive metabolites in Portulaca oleracea. The seeds of P. oleracea were sown, and the plants were cultivated in pots in nursery settings. P. oleracea plants were sprayed with meJA (ranging from 0.1 to 1.0 mM) on the 35th day after sowing (DAS). The plants were harvested on the 60th DAS. The P. oleracea plants elicited with 1.0 mM meJA exhibited the highest plant height (PH), number of leaves (LN), root length (RL), fresh (FW-P), and dry weights of whole plants (DW-P). The highest increase in total anthocyanin (TAC), total chlorophyll (Total Chl), and total carotenoid (CAR) were observed in plants elicited with 0.4 mM meJA. Meanwhile, the highest increase in total phenolic content (TPC) occurred in plants elicited with 0.6 mM meJA, whereas the highest increase in total flavonoid (TFC) and ascorbic acid content (AsA) was noted in plants elicited with 0.8 mM meJA. The lowest decrease in the stress indicators, malondialdehyde (MDA) and hydrogen peroxide (H2O2) was observed in plants elicited with 0.6 mM meJA. Pearson's analysis and Partial Least Squares Regression (PLSR) were employed in exploring the relationships among all essential parameters. It was found that the antioxidant metabolites and enzymes, particularly the total soluble sugar (TSS), proline, chlorophyll a/chlorophyll b ratio (Chl a/Chl b), and superoxide dismutase (SOD) served as the most essential factors in influencing the growth performance of P. oleracea by modulating the total antioxidant activity (Total AOX) and acting as ROS scavengers. Moreover, meJA elicitation led to the distinct expression of various bioactive compounds, amplifying the medicinal properties of P. oleracea. Overall, this research indicates that meJA enhances growth performance and boosts the production of metabolites possessing medicinal values in P. oleracea.