The first high-resolution genetic linkage map of the ancestral octoploid (2n = 8x = 56) strawberry species, Fragaria virginiana, was constructed using segregation data obtained from a pentaploid progeny population. This novel mapping population of size 178 was generated by crossing highly heterozygous F. virginiana hybrid “LB48” as a paternal parent with diploid (2n = 2x = 14) Fragaria vesca “Hawaii 4”. The LB48 linkage map comprises 6055 markers genotyped on the Axiom® IStraw90 strawberry SNP array. The map consists of 28 linkage groups (LGs) organized into seven homoeology groups of four LGs each, and excludes a small 29th LG of undefined homoeology. One member of each homoeology group was assignable to an “A” subgenome associated with ancestral diploid Fragaria vesca, while no other subgenomes were defined. Despite an intriguing discrepancy within homoeology group VI, synteny comparisons with the previously published Fragaria ×ananassa DA × MO linkage map revealed substantial agreement. Following initial map construction, examination of crossover distributions revealed that six of the total 5162 (=29 chromosomes/individual × 178 individuals) chromosomes making up the data set exhibited abnormally high crossover counts, ranging from 15 to 48 crossovers per chromosome, as compared with the overall mean of 0.66 crossovers per chromosome. Each of these six hyper-recombinant (HypR) chromosomes occurred in a different LG and in a different individual. When calculated upon exclusion of the six HypR chromosomes, the canonical (i.e., broadly representative) LB48 map had 1851 loci distributed over a total map length of 1873 cM, while their inclusion increased the number of loci by 130, and the overall map length by 91 cM. Discovery of these hyper-recombinant chromosomes points to the existence of a sporadically acting mechanism that, if identified and manipulable, could be usefully harnessed for multiple purposes by geneticists and breeders.