Bipolarity of the meiotic spindle, required for proper chromosome segregation, is maintained throughout cell division despite rapid microtubule turnover. How this is achieved has remained mysterious, as determining the organization of individual spindle microtubules has been difficult. Here, we develop single-fluorophore speckle imaging to examine microtubule organization in the vertebrate meiotic spindle. We find that the mean length of microtubules is approximately 40% of spindle length. Long and short filaments distribute randomly throughout the spindle and those in close proximity can move in the same direction with highly heterogeneous velocities. The ratio between microtubule and spindle lengths remains unchanged as spindles elongate upon dynein-dynactin inhibition. However, maintaining this ratio depends on proper kinesin-5 function. Our data suggest that force transmission within the spindle must be understood in terms of the crosslinking dynamics of a tiled array of individual filaments, most of which do not span the distance from the pole to the metaphase plate.