Plant and animal populations can adapt to prolonged environmental changes if they have sufficient genetic variation in important phenological traits. The genetic regulation of annual cycles can be studied either via candidate genes or through the decomposition of phenotypic variance by quantitative genetics. Here we combined both approaches to study the timing of migration in a long-distance migrant, the collared flycatcher (Ficedula albicollis). We found that none of the four studied candidate genes (CLOCK, NPAS2, ADCYAP1 and CREB1) had any consistent effect on the timing of six annual cycle stages of geolocator-tracked individuals. This negative result was confirmed by direct observations of males arriving in spring to the breeding site over four consecutive years. Although male spring arrival date was significantly repeatable (R = 0.24 ± 0.08), most was attributable to permanent environmental effects, while the additive genetic variance and heritability was very low (h² = 0.03 ± 0.17 SE). This low value constrains species evolutionary adaptation, and our study adds to warnings that such populations may be threatened, e.g. by ongoing climate change.