Significance A defining goal in genetics is linking variation in DNA sequence to trait evolution between populations and, ultimately, species. Genome sequencing efficiently captures such variation but typically in millions of tiny fragments that omit haplotype or linkage information. We present “haplotagging,” a simple, rapid linked-read sequencing technique that allows high-throughput sequencing without sacrificing haplotype information. We validated this affordable approach for whole-genome haplotyping in large populations. We used haplotagging to investigate the rise of a novel hybrid morph in parallel hybrid zones of two comimetic Heliconius butterfly species in Ecuador. Our results reveal that strikingly parallel divergences in their genomes produced coordinated shifts in haplotype frequencies across the hybrid zone, giving rise to comimetic hybrid morphs in each species.