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ABSTRACT Genetic rescue, specifically translocation to facilitate gene flow among populations and reduce the effects of inbreeding, is an increasingly used approach in conservation. However, this approach comes with trade‐offs, wherein gene flow may reduce fitness when populations have adaptive differentiation (i.e., outbreeding depression). A better understanding of the interaction between isolation, inbreeding, and adaptive divergence in key traits, such as life history traits, will help to inform genetic rescue efforts. Stream‐dwelling salmonids, such as the westslope cutthroat trout (Oncorhynchus lewisi; WCT), are well‐suited for examining these trade‐offs because they are increasingly isolated by habitat degradation, exhibit substantial variation in life history traits among populations, and include many species of conservation concern. However, few genomic studies have examined the potential trade‐offs in inbreeding versus outbreeding depression in salmonids. We used > 150,000 SNPs to examine genomic variation and inbreeding coefficients in 565 individuals across 25 WCT populations that differed in their isolation status and demographic histories. Analyses of runs of homozygosity revealed that several isolated WCT populations had “flatlined” having extremely low genetic variation and high inbreeding coefficients. Additionally, we conducted genome scans to identify potential outlier loci that could explain life history differences among 10 isolated populations. Genome scans identified one candidate genomic region that influenced maximum length and age‐1 to age‐2 growth. However, the limited number of candidate loci suggests that the life history traits examined may be driven by many genes of small effect or phenotypic plasticity. Although adaptive differentiation should be considered, the high inbreeding coefficients in several populations suggest that genetic rescue may benefit the most genetically depauperate WCT populations.