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Abstract Population recovery is a key goal for conservation, but our understanding of how genetic and phenotypic variation, including local adaptation, emerges in recently recolonised or recovering systems is limited. This complicates the conservation of fitness-related traits that support resilience and long-term population viability. We employed single nucleotide polymorphism markers, geometric morphometrics and acoustic telemetry to investigate the recovery of Atlantic salmon ( Salmo salar ) in a large river system, which began more than 40 years ago following presumed extirpation in the mid-1900s. We observed genetic differentiation between Atlantic salmon in different tributaries that may reflect natural recolonisation through straying and/or the recovery of remnant populations previously believed to be extinct. Fine-scale philopatry was found to maintain the genetic divergence between tributaries, as confirmed by genetic assignment and telemetry tracking of returning adults, with some individuals displaying ‘search’ behaviour across tributaries. Despite this population structuring, neither consistent genomic signatures of selection nor morphological divergence were detected, indicating no evidence for early stage local adaptation or for differing selective pressures between tributaries. The patterns instead align with stochastic demographic processes (i.e. founder effects and genetic drift), which was further supported by the low contemporary effective population sizes detected across tributaries. These findings highlight the importance of continued genomic and ecological monitoring during population recovery, as improving environmental conditions may promote the re-establishment of remnant populations and/or facilitate recolonisation. This may, in turn, lead to the formation of reproductively isolated units and, over time, the emergence of locally adapted traits of conservation value for Atlantic salmon and other threatened migratory species.