Friction in nanoscale contacts is determined by the size and structure of the interface that is hidden between the contacting bodies. One approach to investigating the origins of friction is to measure electrical conductivity as a proxy for contact size and structure. However, the relationships between contact, friction and conductivity are not fully understood, limiting the usefulness of such measurements for interpreting dynamic sliding properties. Here, atomic force microscopy (AFM) was used to simultaneously acquire lattice resolution images of the lateral force and current flow through the tip–sample contact formed between a highly oriented pyrolytic graphite (HOPG) sample and a conductive diamond AFM probe to explore the underlying mechanisms and correlations between friction and conductivity. Both current and lateral force exhibited fluctuations corresponding to the periodicity of the HOPG lattice. Unexpectedly, while lateral force increased during stick events of atomic stick-slip, the current decreased exponentially. Molecular dynamics (MD) simulations of a simple model system reproduced these trends and showed that the origin of the inverse correlation between current and lateral force during atomic stick-slip was atom–atom distance across the contact. The simulations further demonstrated transitions between crystallographic orientation during slip events were reflected in both lateral force and current. These results confirm that the correlation between conduction and atom–atom distance previously proposed for stationary contacts can be extended to sliding contacts in the stick-slip regime.