During wakeful rest, individuals make small eye movements during fixation. We examined how these endogenously driven oculomotor patterns impact topography and topology of functional brain networks. We used a dataset consisting of eyes-open resting-state (RS) fMRI data with simultaneous eye tracking. The eye-tracking data indicated minor movements during rest, which correlated modestly with RS BOLD data. However, eye-tracking data correlated well with echo-planar imaging time series sampled from the area of the eye-orbit (EO-EPI), which is a signal previously used to identify eye movements during exogenous saccades and movie viewing. Further analyses showed that EO-EPI data were correlated with activity in an extensive motor and sensorimotor network, including components of the dorsal attention network and the frontal eye fields. Partialling out variance related to EO-EPI from RS data reduced connectivity, primarily between sensorimotor and visual areas. It also produced networks with higher modularity, lower mean connectivity strength, and lower mean clustering coefficient. Our results highlight new aspects of endogenous eye movement control during wakeful rest. They show that oculomotor-related contributions form an important component of RS network topology, and that those should be considered in interpreting differences in network structure between populations or as a function of different experimental conditions. Author Summary We studied how subtle eye movements made during fixation, in absence of any other task, are related to resting-state connectivity measured using fMRI. We used a dataset for which eye tracking and BOLD resting-state were acquired simultaneously. We correlated brain activity with both eye-tracking metrics as well as time series sampled from the area of the eye orbits (EO-EPI). Eye-tracking data correlated well with the EO-EPI data. Furthermore, EO-EPI correlated with BOLD signal in sensorimotor and visual brain systems. Removing variance related to EO-EPI reduced connectivity between sensorimotor and visual areas and resulted in more modular resting-state networks. Our findings show that oculomotor-related contributions are an important component of resting-state network topology, and that they can be studied using EPI data from the eye orbits.