Age-related declines in human skeletal muscle performance may be caused, in part, by decreased responsivity of muscle fibers to calcium (Ca2+). This study examined the contractile properties of single vastus lateralis muscle fibers with various myosin heavy chain (MHC) isoforms (I, I/IIA, IIA and IIAX) across a range of Ca2+ concentrations in 11 young (24.1±1.1years) and 10 older (68.8±0.8years) men and women. The normalized pCa-force curve shifted rightward with age, leading to decreased activation threshold (pCa10) and/or Ca2+ sensitivity (pCa50) for all MHC isoforms examined. In older adults, the slope of the pCa-force curve was unchanged in MHC I-containing fibers (I, I/IIA), but was steeper in MHC II-containing fibers (IIA, IIAX), indicating greater cooperativity compared to young adults. At sub-maximal [Ca2+], specific force was reduced in MHC I-containing fibers, but was minimally decreased in MHC IIA fibers as older adults produced greater specific forces at high [Ca2+] in these fibers. Lessor pCa50 in MHC I fibers independently predicted reduced isokinetic knee extensor power across a range of contractile velocities, suggesting that the Ca2+ response of slow-twitch fibers contributes to whole muscle dysfunction. Our findings show that aging attenuates Ca2+ responsiveness across fiber types and that these cellular alterations may lead to age-related reductions in whole muscle power output.