Knowledge of the genetic variances and covariances of traits (the G-matrix) is fundamental for the understanding of evolutionary dynamics of populations. Despite its essential importance in evolutionary studies, empirical tests of the temporal stability of the G-matrix in natural populations are few. We used a 25-year-long individual-based field study on almost 7000 breeding attempts of the collared flycatcher (Ficedula albicollis) to estimate the stability of the G-matrix over time. Using animal models to estimate G for several time periods, we show that the structure of the time-specific G-matrices changed significantly over time. The temporal changes in the G-matrix were unpredictable, and the structure at one time period was not indicative of the structure at the next time period. Moreover, we show that the changes in the time-specific G-matrices were not related to changes in mean trait values or due to genetic drift. Selection, differences in acquisition/allocation patterns or environment-dependent allelic effects are therefore likely explanations for the patterns observed, probably in combination. Our result cautions against assuming constancy of the G-matrix and indicates that even short-term evolutionary predictions in natural populations can be very challenging.