Profound sea ice loss is rapidly transforming coupled social-ecological Arctic marine systems. However, explicit impacts to harvesting of traditional resources for coastal Indigenous communities remain largely unquantified, particularly where the primary research questions are posed by the Indigenous community as a result of emerging approaches such as knowledge co-production. Here, we directly link reduced sea ice coverage to decreasing harvesting opportunities for ugruk (bearded seal, Erignathus barbatus) as a component of a partnership among a multidisciplinary team of scientists, Indigenous Elder Advisory Council, and sovereign Indigenous tribe in northwest Alaska, USA. We collaboratively established research questions, coordinated data collection, and interpreted results to understand the causes and consequences of changing ugruk harvests for the community of Qikiqtaġruk (Kotzebue). The duration of spring ugruk hunts by the Qikiqtaġruŋmiut declined significantly during 2003–2019 due to a shift (∼3 weeks earlier) in the timing of regional sea ice breakup. Harvests now cease ∼26 d earlier than in the past decade. Using historical sea ice records, we further demonstrate that ice coverage in May now resembles conditions that were common in July during the mid-20th century. Overall, we show that climate change is constraining hunting opportunities for this traditional marine resource, although Qikiqtaġruŋmiut hunters have so far been able to offset a shortened season with changes in effort. Notwithstanding recent hunting success in unprecedentedly sparse ice conditions, accessibility to traditional resources remains a prominent concern for many Arctic communities. Management and policy decisions related to Arctic marine mammal resources, such as ugruk, are therefore also interwoven with food security, well-being, and culture of Indigenous communities. Hence, research that originates with Indigenous sovereignty over the entire research process, such as demonstrated here, has the potential to also lead to more inclusive, sustainable, and equitable outcomes in the face of rapid and accelerating Arctic change.