The positioning of antennae in insects involves aspects of both stability and flexibility. On short timescales, rapid proprioceptive feedback about the position of the antennae is used to keep them stable at a preferred position, hereafter referred to as the set-point. On longer timescales, this set-point is flexibly modulated by sensory inputs from multiple modalities including vision and airflow. Whereas the antennal stabilization reflex has been investigated using control theoretic techniques and neural circuit models, the mechanisms that underlie modulation of antennal set-point are not well understood. In the current study, we investigate the modulation of antennal set-point using the airflow-dependent antennal positioning behavior in the Oleander hawkmoth, Daphnis nerii. Our previous work has shown that airflow-dependent control of antennal position requires sensory inputs from the Johnston’s organ (JO), an antennal mechanosensory organ that senses vibrations of the antennae. Here, using behavioral experiments, we investigate the role of individual JOs in modulating the set-point of both antennae. We find that unilateral restriction of JOs disrupts the set-points of both antennae for different airflows. To further characterize this, we used a finely calibrated stimulus setup to deliver precise flagellar vibrations to the antennae while simultaneously recording from the extrinsic muscles of both antennae. By pooling behavioral and electrophysiological data, we aim to characterize how the sensory inputs from the JOs tune the antennal set-point and modulate antennal positioning.