The objective of this study was to quantify the genetic variation in normal and atypical progesterone profiles and investigate if this information could be useful in an improved genetic evaluation for fertility for dairy cows. The phenotypes derived from normal profiles included cycle length traits, including commencement of luteal activity (C-LA), interluteal interval, luteal phase length. and interovulatory interval. In total, 44,977 progesterone test-day records were available from 1,612 lactations on 1,122 primiparous and multiparous Holstein-Friesian cows from Ireland, the Netherlands, Sweden, and the United Kingdom. The atypical progesterone profiles studied were delayed cyclicity, prolonged luteal phase, and cessation of cyclicity. Variance components for the atypical progesterone profiles were estimated using a sire linear mixed model, whereas an animal linear mixed model was used to estimate variance components for the cycle length traits. Heritability was moderate for delayed cyclicity (0.24 ± 0.05) and C-LA (0.18 ± 0.04) but low for prolonged luteal phase (0.02 ± 0.04), luteal phase length (0.08 ± 0.05), interluteal interval (0.08 ± 0.14), and interovulatory interval (0.03 ± 0.04). No genetic variation was detected for cessation of cyclicity. Commencement of luteal activity, luteal phase length, and interovulatory interval were moderately to strongly genetically correlated with days from calving to first service (0.35 ± 0.12, 0.25 ± 0.14, and 0.76 ± 0.24, respectively). Delayed cyclicity and C-LA are traits that can be important in both genetic evaluations and management of fertility to detect (earlier) cows at risk of compromised fertility. Delayed cyclicity and C-LA were both strongly genetically correlated with milk yield in early lactation (0.57 ± 0.14 and 0.45 ± 0.09, respectively), which may imply deterioration in these traits with selection for greater milk yield without cognizance of other traits.