Sogatella furcifera is an agricultural pest of great concern in China and Southeast Asian countries. However, the lack of accurate and complete reference genome resources has hindered the understanding of immunity and evolution of S. furcifera. Here, we utilized Nanopore sequencing to generate a chromosome-level assembly and annotation of the S. furcifera genome (0.64 Gb), with a GC content of 34.25%. This genome comprised 15 chromosomes covering 95.04% of the estimated genome size, together with an additional 624 small scaffolds making up the remaining 4.96% of the genome of S. furcifera. A total of 24,669 protein-coding genes as well as 1211 long noncoding RNA and 7595 circular RNA transcripts were well annotated and predicted. Comparative genomic analysis revealed the rapidly evolved genes associated with multiple immune-related pathways in S. furcifera, which may be responsible for its rapid evolutionary adaptation. In addition, 14 immune genes in the classic immune pathways were selected for functional validation through RNA interference experiments, demonstrating the antiviral effects of Dorsal and Dif genes in S. furcifera. Genome resequencing of 44 individuals from 12 geographic populations revealed an absence of population structures and frequent gene flow among all populations. Sweep analysis indicated that 2926 genes were under natural selection and significantly enriched in several biological processes of morphogenesis and immunity. The first systematic identification of immune genes and noncoding RNAs from chromosome-level genome assembly plus the comparative and population genomic analysis will provide more insights into the understanding of the immunity and evolutionary adaptation of S. furcifera.