We critically discuss whether and under what conditions Lifshitz theory may be used to describe thermal Casimir-Polder forces on atoms or molecules. An exact treatment of the atom-field coupling reveals that for a ground-state atom (molecule), terms associated with virtual-photon absorption lead to a deviation from the traditional Lifshitz result; they are identified as a signature of non-equilibrium dynamics. Even the equilibrium force on a thermalized atom (molecule) may be overestimated when using the ground-state polarizability instead of its thermal counterpart. In all of these areas, a thorough understanding of dispersion forces under realistic conditions must account for their temperature dependence induced by thermal photons [6]. A series of high-precision experiments [7] has triggered a renewed interest in this thermal Casimir force [8] by opening the perspective of its experimental investigation [9]. It was noticed that, depending on the model chosen to describe the metal response, Lifshitz theory can yield different answers for the temperature dependence of the Casimir energy between two metal plates [10]. The resulting debate concerning the correct description of the thermal Casimir force [11] will ultimately have to be settled by experiments. Non-equilibrium situations of two plates of different temperatures have recently been suggested as sensitive probes to the quantum electrodynamics (QED) of the Casimir effect [12].The CP force on single atoms can be measured indirectly via spectroscopic means; clear evidence for thermal frequency shifts has been found for atoms inside a cavity [13] and their signature has been detected in the interaction of atoms with a sapphire surface [14]. The novel non-equilibrium CP forces predicted for the case of different surface and environment temperatures [15] have recently been observed via their effect on the centerof-mass oscillations of a trapped Bose-Einstein condensate [16]. While some theoretical studies of the thermal CP force are based on a QED treatment of the atomfield coupling [17,18], the vast majority of investigations invokes a macroscopic calculation using Lifshitz theory [6,19,20] or a linear-response description of the atom [15,21] (leading to equivalent results).The macroscopic approach to the CP force is based on a very close relation between Casimir and CP forces. It is the validity of this one-to-one correspondence and its results for the CP force that we intend to investigate in this Letter, so let us briefly recount the argument in its traditional form: Generalizing the famous Lifshitz result for two plates [6], the thermal Casimir force on a homogeneous body of arbitrary shape occupying a volume V in free space due to the presence of another body can be given as a Matsubara sum [22,23] with Matsubara frequencies ξ N = 2πk B T N/ . Here, Gis the scattering part of the classical Green tensorassociated with the bodies that are characterized by their dielectric permittivity ε(r, ω). The result (1) can be obtained from the zero-temperature force b...