Capturing the genetic diversity of wild relatives is crucial for improving crops because wild species are valuable sources of agronomic traits that are essential to enhance the sustainability and adaptability of domesticated cultivars. Genetic diversity across a genus can be captured in super-pangenomes, which provide a framework for interpreting genomic variations. Here we report the sequencing, assembly, and annotation of nine wild North American grape genomes, which were phased and scaffolded at chromosome scale. We generated a reference-unbiased super-pangenome using pairwise whole-genome alignment methods, revealing the full resolution of genomic diversity among wild grape species from sequence to gene level. The pangenome graph captured genomic variation between haplotypes within a species and across the different species, and it accurately assessed the similarity of hybrids to their parents. The species selected to build the pangenome ensured a comprehensive representation of the genus, as illustrated by capturing known allelic variants in the sex-determining region and for Pierce's disease resistance loci. Using pangenome-wide association analysis (pan-GWAS), we demonstrated the utility of the super-pangenome by effectively mapping short-reads from genus-wide samples and identifying loci associated with salt tolerance in natural populations of grapes. This study highlights how a reference-unbiased super-pangenome can reveal the genetic basis of the adaptive traits from wild relatives, potentially accelerating crop breeding research.