The genetic diversity in Brassica napus (canola, rapeseed) is limited because of few hybridization events and selection for important oil quality traits. One possible means of overcoming this challenge is through resynthesizing B. napus hybrids by crossing the diploid parents in order to broaden its gene pool. However, resynthesized B. napus lines are often unstable and infertile, unlike B. napus cultivars. Meiotic stability in established B. napus may have arisen through allele inheritance from the progenitor species. We tested this hypothesis by characterizing 41 resynthesized B. napus lines produced by crosses between eight B. rapa and eight B. oleracea lines for copy number variation resulting from non-homologous recombination events, allele inheritance, and fertility. We resequenced eight B. rapa and five B. oleracea parent accessions, and analyzed the allelic variation in a list of meiosis gene homologs. SNP genotyping was performed using the Illumina Infinium Brassica 60K array for three individuals per line. Self-pollinated seed-set and genome stability (number of copy number variants) were significantly affected by the interaction between both B. rapa and B. oleracea parental genotypes. We identified two putative meiosis gene candidates ( HEI10 and MCM8 ) which were significantly associated with meiosis and/or fertility as well as genome stability. Our results support the hypothesis that allelic variants inherited from parental genotypes affect genome stability and fertility in resynthesized rapeseed.