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Raw sequencing reads of ancient samples produced for this study have been deposited in the European Nucleotide Archive under accession no. PRJEB46830. Modern mitochondrial genomes generated as part of this study have been deposited in GenBank, accession nos. MZ846240 to MZ848095., Orkney was a major cultural center during the Neolithic, 3800 to 2500 BC. Farming flourished, permanent stone settlements and chambered tombs were constructed, and long-range contacts were sustained. From ∼3200 BC, the number, density, and extravagance of settlements increased, and new ceremonial monuments and ceramic styles, possibly originating in Orkney, spread across Britain and Ireland. By ∼2800 BC, this phenomenon was waning, although Neolithic traditions persisted to at least 2500 BC. Unlike elsewhere in Britain, there is little material evidence to suggest a Beaker presence, suggesting that Orkney may have developed along an insular trajectory during the second millennium BC. We tested this by comparing new genomic evidence from 22 Bronze Age and 3 Iron Age burials in northwest Orkney with Neolithic burials from across the archipelago. We identified signals of inward migration on a scale unsuspected from the archaeological record: As elsewhere in Bronze Age Britain, much of the population displayed significant genome-wide ancestry deriving ultimately from the Pontic-Caspian Steppe. However, uniquely in northern and central Europe, most of the male lineages were inherited from the local Neolithic. This suggests that some male descendants of Neolithic Orkney may have remained distinct well into the Bronze Age, although there are signs that this had dwindled by the Iron Age. Furthermore, although the majority of mitochondrial DNA lineages evidently arrived afresh with the Bronze Age, we also find evidence for continuity in the female line of descent from Mesolithic Britain into the Bronze Age and even to the present day., We thank Steve Birch, Jenny Murray, and Sue Black for help with samples; Harald Ringbauer for advice on hapROH; and Joyce Richards for comments on an early draft. Excavations at LoN and KoS are directed by H.M. and G.W., EASE (Environment and Archaeology Services), grant funded by Historic Environment Scotland. M. Ni Challanain, M. McCormick, and D. Gooney undertook osteological identifications and sample selection. K.D., M.G.B.F, P.J., M.S., G.O.-G, A.F., and S.R. were supported by a Leverhulme Trust Doctoral Scholarship program awarded to M.B.R. and M.P. DNA sequencing was also supported by the UK Natural Environment Research Council Biomolecular Analysis Facility (NBAF) at the University of Liverpool, under NBAF Pilot Scheme NBAF685, awarded to C.J.E. whilst at the University of Oxford. P.S., M.P., and M.B.R. acknowledge FCT (Fundação para a Ciência e a Tecnologia) support through project PTDC/EPH-ARQ/4164/2014, partially funded by FEDER (Fundo Europeu de Desenvolvimento Regional) funds (COMPETE 2020 project 016899). PS was supported by FCT, European Social Fund, Programa Operacional Potencial Humano, and the FCT Investigator Programme and acknowledges FCT/MEC (Ministério da Educação e Ciência) for support to CBMA through Portuguese funds (PIDDAC: Programa de Investimentos e Despesas de Desenvolvimento da Administração Central)—PEst-OE/BIA/UI4050/2014. V.M. and D.G.B. acknowledge the Science Foundation Ireland/Health Research Board/Wellcome Trust Biomedical Research Partnership Investigator Award No. 205072 to D.G.B., “Ancient Genomics and the Atlantic Burden.” The ORCADES was supported by the Chief Scientist Office of the Scottish Government (CZB/4/276, CZB/4/710), a Royal Society University Research Fellowship to J.F.W., the MRC (Medical Research Council) Human Genetics Unit quinquennial programme “QTL in Health and Disease,” Arthritis Research UK, and the EU FP6 EUROSPAN project (contract no. LSHG-CT-2006-018947). The Edinburgh Clinical Research Facility, University of Edinburgh, performed DNA extractions and the Sanger Institute performed whole-genome sequencing. The Viking Health Study–Shetland (VIKING) was supported by the MRC Human Genetics Unit quinquennial programme grant “QTL in Health and Disease.” DNA extractions were performed at the Edinburgh Clinical Research Facility, University of Edinburgh. Whole genome sequencing was supported by the Scottish Genomes Partnership award from the Chief Scientist Office of the Scottish Government and the MRC (grant reference SGP/1) and the MRC Whole Genome Sequencing for Health and Wealth Initiative (MC/PC/15080). We acknowledge Wellcome Trust funding (098051) for the ORCADES whole-genome sequencing. J.F.W. acknowledges support from the MRC Human Genetics Unit programme grant, “Quantitative traits in health and disease” (U. MC_UU_00007/10). We also acknowledge the invaluable contributions of the research nurses in Orkney and Shetland, the administrative team in Edinburgh, and the people of Orkney and Shetland.