Sugar beet (Beta vulgaris L.) shows potential as an energy crop for cadmium (Cd) phytoremediation. To elucidate its in vivo response strategy to Cd exposure, seedlings were treated with 1, 3, and 5 mmol/L CdCl2 (Cd-1, Cd-3, and Cd-5) for 6 h, using 0 mmol/L CdCl2 (Cd-0) as the control. The results showed that Cd-3 promoted a unique “hormesis” effect, leading to superior growth performance, increased levels of chlorophyll, soluble protein, and SOD activity, and reduced MDA content in sugar beet, compared to Cd-1, Cd-5, and even Cd-0. GO and KEGG enrichments and PPI networks of transcriptomic analysis revealed that the differentially expressed genes (DEGs) were primarily involved in lipid metabolism, cellular protein catabolism, and photosynthesis. Notably, the MAPK signaling pathway was significantly enriched only under Cd-3, with the up-regulation of ABA-related core gene BvPYL9 and an increase in ABA content after 6 h of Cd exposure. Furthermore, overexpression of BvPYL9 in Arabidopsis thaliana (OE-1 and OE-2) resulted in enhanced growth (fresh weight, dry weight, and root length), as well as higher ABA and soluble protein contents under different Cd treatments. Cd-induced transcriptional responses of BvPYL9 were also evident in OE-1 and OE-2, especially at 10 µmol/L, indicated by qRT-PCR. These findings suggest that ABA-mediated MAPK signaling pathway is activated in response to Cd toxicity, with BvPYL9 being a key factor in the cascade effects for the Cd-induced hormesis in sugar beet.