In the northeast United States, subadult deer ticks feeding on white-footed mice are thought to drive the force of transmission of Borrelia burgdorferi (B. burgdorferi), the agent of Lyme disease. However, control measures targeting mice have produced inconsistent results, suggesting that other animals are significant contributors to enzootic transmission. Such contributions have previously been difficult to quantify. We used a retrotransposon-based host blood meal assay to measure the relative contribution of hosts to enzootic B. burgdorferi transmission at two insular sites in Massachusetts. Over 6 years, we identified mice and deer as the most common larval hosts at our Nantucket Island site. Infected nymphal ticks were derived mainly from mice (35%) and shrews (31%), despite shrews having fed only 12% of larvae. Deer were identified in 19% of the infected nymphs, despite their known reservoir incompetence. Shrews were consistently the most important host in our Martha's Vineyard site and were identified as the source of 41% of nymphs overall and 39% of the infected nymphs. Sciurids were variable contributors, feeding from 4% to 42% of the larval ticks each year, and contributed no infected nymphs in 2020 and as many as 83% in 2023. We conclude that host contributions to feeding larval ticks change over time and within sites and that shrews may be more influential than mice at some sites. Shrews, sciurids, and even deer may contribute to B. burgdorferi maintenance. Hosts that apparently feed a minor proportion of ticks can have a major impact on the force of B. burgdorferi transmission.