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Autophagy is a common physiological process in organisms, including higher plants. The <i>ATG8</i> subfamily, the core member of the autophagy-related gene (ATG) family, plays a key role in plant growth and development and nutrient stress responses. However, the core <i>ATG8</i> homologs and their roles in stress resistance remain elusive in allotetraploid rapeseed (AACC, <i>Brassica napus</i> L.). In this study, we identified 29 <i>ATG8</i> subgroup members, consisting of three phylogenetic clades, based on the analysis of genomic annotation and conserved motifs. Differential transcriptional responses of <i>BnaATG8s</i> to salt stress, nitrogen limitation, and other nutrient stresses were investigated, and we identified <i>BnaA8.ATG8F</i> as the core <i>ATG8</i> member through gene co-expression network analysis. Decreased <i>BnaA8.ATG8F</i> expression repressed the salt tolerance of transgenic rapeseed plants by significantly reducing the root Na⁺ retention under salt stress. Moreover, downregulation of <i>BnaA8.ATG8F</i> increased nitrogen (N) limitation sensitivity of transgenic rapeseed plants through decreasing N uptake, translocation, and enhancing N remobilization under nitrogen starvation. In summary, we identified the core <i>ATG8</i> homologs and characterized their physiological and molecular mechanisms underlying salt stress tolerance and nitrogen limitation adaptation. Our results may provide elite genetic resources for the genetic improvement of nutrient stress tolerance in rapeseed.