Pacific lamprey (Entosphenus tridentatus) is a culturally important and imperiled anadromous fish with a parasitic ocean phase. Biological uncertainties challenge restoration efforts and life-history research is needed to explain observed trait variation and inform management actions. Using two new whole genome assemblies and genotypes from 7,716 single nucleotide polymorphism (SNP) loci in 518 individuals from across the species range, we identified four large regions of high genomic divergence (on chromosomes 01, 02, 04, and 22). We genotyped a subset of 302 broadly distributed SNPs in 2,145 individuals for genotype-by-phenotype trait associations for adult body size, sexual maturity, migration distance and timing, adult swimming ability, and larval growth. Body size traits were strongly associated with SNPs on chromosomes 02 and 04. Moderate associations also implicated SNPs on chromosome 01 as being associated with variation in female maturity. Using genotypic frequencies of candidate SNPs for female maturity and body size, we extrapolated a heterogeneous spatiotemporal distribution of these traits based on independent datasets of larval and adult collections. These maturity and body size results guide future studies to validate these predicted phenotypic distributions across the geographic range and elucidate factors driving regional optimization of these traits for fitness.