Established allopolyploids are known to be genomically stable and fertile. However, in contrast, most newly resynthesized allopolyploids are infertile and meiotically unstable. Identifying the genetic factors responsible for genome stability in newly formed allopolyploid is key to understanding how 2 genomes come together to form a species. One hypothesis is that established allopolyploids may have inherited specific alleles from their diploid progenitors which conferred meiotic stability. Resynthesized Brassica napus lines are often unstable and infertile, unlike B. napus cultivars. We tested this hypothesis by characterizing 41 resynthesized B. napus lines produced by crosses between 8 Brassica rapa and 8 Brassica oleracea lines for copy number variation resulting from nonhomologous recombination events and fertility. We resequenced 8 B. rapa and 5 B. oleracea parent accessions and analyzed 19 resynthesized lines for allelic variation in a list of meiosis gene homologs. SNP genotyping was performed using the Illumina Infinium Brassica 60K array for 3 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 13 putative meiosis gene candidates which were significantly associated with frequency of copy number variants and which contained putatively harmful mutations in meiosis gene haplotypes for further investigation. Our results support the hypothesis that allelic variants inherited from parental genotypes affect genome stability and fertility in resynthesized rapeseed.