This protocol describes a generalizable, long-read, low-input metagenomic sequencing approach ('VirION') for the survey of viral communities. A significant obstacle in adopting long-read technology for viral metagenomics lies in obtaining the amount of DNA required; e.g. viral DNA extraction from 20 L of seawater yields far less than the micrograms of DNA recommended for efficient long-read sequencing. To overcome this limitation, we developed a Long-Read Linker-Amplified Shotgun Library approach for long-read viral metagenomics. The VirION method has been demonstrated to be as relatively quantitative as short-read methods, and analyses that combined VirION long-read data with Illumina, short-read data, captured many abundant and ubiquitous viral genomes that were missed by short-read assemblies. This approach was also shown to have overcome issues of microdiversity, and to have captured more genomic islands than short-read assemblies. Thus, VirION provides a high throughput and cost-effective alternative to fosmid and single-virus genomic approaches.