Understanding the extent to which diversity at immunologically important genes is reduced by demographic perturbations such as population bottlenecks, and the resulting consequences this has on individual fitness, is of fundamental importance for the effective management of genetic resources in natural populations. Toll-like receptors are key immunological genes with well-established links to fitness. Here, levels of allelic diversity and heterozygosity at the toll-like receptor 4 locus (Tlr4) were characterised across 280 water voles (Arvicola amphibius) from an isolated, island population in north west Scotland that went through a severe population bottleneck between 2004 and 2006 that eroded neutral microsatellite variation. Two functional Tlr4 alleles were resolved prior to the population crash at frequencies close to parity and an excess of heterozygote genotypes relative to Hardy-Weinberg expectations. Through the population bottleneck both alleles were retained with genotype frequencies conforming to Hardy-Weinberg expectations. Tlr4 genotype was significantly associated with gamasid mite, flea (Megabothris walkeri) and sheep tick larva (Ixodes ricinus) burdens among individuals, suggesting a mechanism through which parasite mediated selection could affect Tlr4 diversity. The results are examined with recourse to the extent that they are consistent with the effects of genetic drift and balancing selection, and their significance is discussed in relation to identifying target genes that assay ecological and adaptively meaningful genetic variation in a conservation context.