Commercial aircraft are becoming highly automated, but pilots must take control if automation systems fail. Failures can be due to known limitations (system-limit failures) or unforeseen malfunctions (system-malfunction failures). This study quantifies the impact of these failures on response performance and monitoring behavior, considering four levels of operational proficiency. In a flight simulator with pitch, roll, and yaw, 24 participants experienced both types of failures at different proficiency levels. The results showed that system-malfunction failure response times were 3.644, 2.471, 2.604, and 4.545 times longer than system-limit failure response times at proficiency levels 1 to 4. Monitoring behaviors (fixation duration, saccade duration, fixation rate) differed between failure types and proficiency levels. Considering these differences in response performance and monitoring behavior between failure types, it is important to differentiate between system-limit and system-malfunction failures in the literature and not overlook the influence of proficiency. Furthermore, due to the unpredictability of system-malfunctions, it is crucial to develop pilots’ psychological models and training theories regarding the operation of automated systems, fostering their core competency to excel in handling unknown situations.