Slender body theory facilitates computational simulations of thin fibers immersed in a viscous fluid by approximating each fiber using only the geometry of the fiber centerline curve and the line force density along it. However, it has been unclear how well slender body theory actually approximates Stokes flow about a thin but truly three-dimensional fiber, in part due to the fact that simply prescribing data along a 1D curve does not result in a well-posed boundary value problem for the Stokes equations in ℝ3. Here, we introduce a PDE problem to which slender body theory (SBT) provides an approximation, thereby placing SBT on firm theoretical footing. The slender body PDE is a new type of boundary value problem for Stokes flow where partial Dirichlet and partial Neumann conditions are specified everywhere along the fiber surface. Given only a 1D force density along a closed fiber, we show that the flow field exterior to the thin fiber is uniquely determined by imposing a fiber integrity condition: the surface velocity field on the fiber must be constant along cross sections orthogonal to the fiber centerline. Furthermore, a careful estimation of the residual, together with stability estimates provided by the PDE well-posedness framework, allows us to establish error estimates between the slender body approximation and the exact solution to the above problem. The error is bounded by an expression proportional to the fiber radius (up to logarithmic corrections) under mild regularity assumptions on the 1D force density and fiber centerline geometry.