The fluctuation-dissipation theorem is a fundamental result in statistical physics that establishes a connection between the response of a system subject to a perturbation and the fluctuations associated with observables in equilibrium. Here we derive its version within a resource-theoretic framework, where one investigates optimal quantum state transitions under thermodynamic constraints. More precisely, we first characterize optimal thermodynamic distillation processes, and then we prove a relation between the amount of free energy dissipated in such processes and the free-energy fluctuations of the initial state of the system. Our results apply to initial states given by either asymptotically many identical pure systems or an arbitrary number of independent energy-incoherent systems, and they allow not only for a state transformation but also for the change of Hamiltonian. The fluctuation-dissipation relations we derive enable us to find the optimal performance of thermodynamic protocols such as work extraction, information erasure, and thermodynamically free communication, up to second-order asymptotics in the number N of processed systems. We thus provide a first rigorous analysis of these thermodynamic protocols for quantum states with coherence between different energy eigenstates in the intermediate regime of large but finite N.