The ongoing deficit of fresh water resource in rice growing regions has made the selection of water-saving and drought-resistance rice (WDR) a crucial factor in developing sustainable cultivation. HuHan2B, a new japonica maintainer for WDR breeding, had the same yield potential as recurrent parent HanFengB but showed improved drought resistance in fields. We investigated the genomic content accumulation and candidate genes passed from parent to offspring using the genomic and transcriptomic approaches. The genomic constitution indicated that the genetic similarity was 84% between HuHan2B and HanFengB; additionally, 7,256 genes with specific alleles were inherited by HuHan2B from parents other than HanFengB. The differentially expressed genes (DEGs) under drought stress showed that biological function was significantly enriched for transcript regulation in HuHan2B, while the oxidation-reduction process was primarily enriched in HanFengB. Furthermore, 36 DEGs with specific inherited alleles in HuHan2B were almost involved in the regulatory network of TFs and target genes. These findings suggested that major-effect genes were congregated and transformed into offspring in manner of interacting network by breeding. Thus, exploiting the potential biological function of allelic-influencing DEGs would be of great importance for improving selection efficiency and the overall genetic gain of multiple complex traits.