Water is characterized by strong intermolecular hydrogen bonds (H-bonds) between molecules. The two hydrogen atoms in one water molecule can form H-bonds of dissimilar length. Although intimately connected to water’s anomalous properties, the details and the origins of the asymmetry have remained elusive. We study water’s H-bonds using the O-D stretching vibrations as sensitive reporters of H-bonding of D2O and HOD in dimethylformamide. Broader inhomogeneous linewidths of the OD band of HOD compared to the symmetric and asymmetric OD stretching modes of D2O together with density functional theory calculations provide evidence for markedly anti-correlated H-bonds: water preferentially forms one weak and one strong H-bond. Coupling peaks in the spectra for D2O directly demonstrate anti-correlated H-bonds and these anti-correlations are modulated by thermal motions of water on a sub-picosecond timescale. Experimentally inferred H-bond distributions suggest that the anti-correlations are a direct consequence of the H-bonding potential of XH2 groups, which we confirm for the ND2 group of urea. These structural and dynamic insights into H-bonding are essential for understanding the relationship between the H-bonded structure and phase behavior of water.