The aquatic planorbid snail Biomphalaria glabrate is one of the most intensively-studied mollusks due to its role in the transmission of schistosomiasis. Its 916 Mb genome has recently been sequenced and annotated, but it remains poorly assembled. Here we used targeted capture markers to map over 10,000 B. glabrate scaffolds in a linkage cross of 94 F1 offspring, generating 24 linkage groups. We added additional scaffolds to these linkage groups based on linkage disequilibrium analysis of targeted capture and whole-genome sequences of 96 unrelated snails. Our final linkage map consists of 18,613 scaffolds comprising 515 Mb, representing 56% of the genome and 75% of genic and nonrepetitive regions. There are 18 large (>10 Mb) linkage groups, likely representing the expected 18 haploid chromosomes, and more than 50% of the genome has been assigned to linkage groups of at least 17 Mb. Comparisons with other gastropod genomes reveal patterns of synteny and chromosomal rearrangements. Linkage relationships of key immune-relevant genes may help clarify snail-schistosome interactions. By focusing on linkage among genic and nonrepetitive regions, we have generated a useful resource for associating snail phenotypes with causal genes, even in the absence of a complete genome assembly. A similar approach could potentially improve numerous poorly-assembled genomes in other taxa. This map will facilitate future work on this host of a serious human parasite.