In this study we employed nanopore whole genome sequencing to analyze the resistance genes, genomic islands and prophage DNA in two multidrug resistant E. rhusiopathiae strains, i.e., 670 and 147, isolated from domestic geese. MLST profiles and core-genome phylogeny were determined to assess strain relatedness. In strain 670 (serotype 8, ST 113), a novel 53 kb prophage φEr670 carrying the lnuB and lsaE resistance genes was identified. Regions highly homologous to the φEr670 prophage were detected in 36 of 586 (6.14%) publicly available E. rhusiopathiae genomes, as well as in some other Gram-positive bacteria, and usually contained resistance genes. E. rhusiopathiae strain 147 (serotype 5, ST 243) was found to contain a composite 98 kb genomic island (GI_Er147) carrying the ant(6)-Ia and spw genes, as well as gene encoding a putative lincosamide nucleotidyltransferase designated lnu(J) and a vat family gene encoding a putative streptogramin A O-acetyltransferase. The lnu(J) gene exhibited 83.6% homology to the lnu(D) gene, and lnu(J)-positive E. rhusiopathiae strains displayed intermediate susceptibility to lincomycin. Vat-positive strain 147 and vat-negative E. rhusiopathiae strains showed similar susceptibility to quinupristin/dalfopristin. The presence of the Tn916 transposon carrying the tetM gene was confirmed in the genomes of both E. rhusiopathiae strains; in strain 147, however, Tn916 was located within ICEEr1012. Based on analyses of additional E. rhusiopathiae genomes, the integration sites of Tn916, ICEEr1012, and GI_Er147 were identified as genomic “hot spots,” contributing to the genome plasticity of E. rhusiopathiae. Prophage φEr670 and GI_Er147 as well as the Tn916 transposon and ICEEr1012 are most likely responsible for the dissemination of resistance genes in E. rhusiopathiae. Prophages highly homologous to φEr670 act as carriers of resistance genes in various Gram-positive bacteria. However, the transferability of the identified genetic elements and the functional role of the lnu(J) gene require further investigation. This study provides new insights into the diversity of MGEs in E. rhusiopathiae and advances understanding of the genomic mechanisms driving antimicrobial resistance in Gram-positive bacteria.