We studied the relationship between the force and velocity of microtubule sliding in demembranated sperm flagella of the sea urchin, Hemicentrotus pulcherrimus, under auxotonic conditions following a quick release of the tension between sliding microtubules. The shape of the force-velocity curve was independent of the concentration of Mg-ATP over the range of 3.7 to 350 μM and appeared either linear or was the reverse of the hyperbolic curve seen for muscle. The power, calculated as the product of velocity and force, passed through a peak at c. 0.7 F_max (the maximal isometric force). Thus, the maximal power is attained at a larger relative load than in muscle. The sliding velocity at 0.1 F_max showed a hyperbolic dependence on Mg-ATP concentration, with a K_m of 210 μM and a V_max of 19 μm•sec^-1. The maximal force did not significantly change over the Mg-ATP concentration range of 3.7 to 350 μM. These results are discussed in terms of a crossbridge model similar to the one originally proposed by Huxley. It is suggested that the dynein crossbridge cycle is characterized by a relatively rapid rate of attachment and a relatively slow rate of detachment.