Camelina is an ancient oilseed crop that produces an oil rich in cis-9,cis-12 18:2 (linoleic acid, LA) and cis-9,cis-12,cis-15 18:3 (α-linolenic acid, ALA); however, reports on the use of camelina oil (CO) for ruminants are limited. The present study investigated the effects of incremental CO supplementation on animal performance, milk fatty acid (FA) composition, and milk sensory quality. Eight Finnish Ayrshire cows (91 d in milk) were used in replicated 4 × 4 Latin squares with 21-d periods. Treatments comprised 4 concentrates (12 kg/d on an air-dry basis) based on cereals and camelina expeller containing 0 (control), 2, 4, or 6% CO on an air-dry basis. Cows were offered a mixture of grass and red clover silage (RCS; 1:1 on a dry matter basis) ad libitum. Incremental CO supplementation linearly decreased silage and total dry matter intake, and linearly increased LA, ALA, and total FA intake. Treatments had no effect on whole-tract apparent organic matter or fiber digestibility and did not have a major influence on rumen fermentation. Supplements of CO quadratically decreased daily milk and lactose yields and linearly decreased milk protein yield and milk taste panel score from 4.2 to 3.6 [on a scale of 1 (poor) to 5 (excellent)], without altering milk fat yield. Inclusion of CO linearly decreased the proportions of saturated FA synthesized de novo (4:0 to 16:0), without altering milk fat 18:0, cis-9 18:1, LA, and ALA concentrations. Milk fat 18:0 was low (<5 g/100 g of FA) across all treatments. Increases in CO linearly decreased the proportions of total saturates from 58 to 45 g/100 g of FA and linearly enriched trans-11 18:1, cis-9,trans-11 18:2, and trans-11,cis-15 18:2 from 5.2, 2.6, and 1.7 to 11, 4.3, and 5.8 g/100 g of FA, respectively. Furthermore, CO quadratically decreased milk fat trans-10 18:1 and linearly decreased trans-10,cis-12 18:2 concentration. Overall, milk FA composition on all treatments suggested that one or more components in camelina seeds may inhibit the complete reduction of 18-carbon unsaturates in the rumen. In conclusion, CO decreased the secretion of saturated FA in milk and increased those of the trans-11 biohydrogenation pathway or their desaturation products. Despite increasing the intake of 18-carbon unsaturated FA, CO had no effect on the secretions of 18:0, cis-9 18:1, LA, or ALA in milk. Concentrates containing camelina expeller and 2% CO could be used for the commercial production of low-saturated milk from grass-and RCS-based diets without major adverse effects on animal performance.