Circadian rhythms are endogenous cellular patterns that associate multiple physiological and molecular functions with time. The Neurospora circadian system contains at least three oscillators: the FRQ/WC-dependent circadian oscillator (FWO), whose core components are the FRQ, WC-1, WC-2, FRH, and FWD-1 proteins; the WC-dependent circadian oscillator (WC-FLO); and one or more FRQ/ WC-independent oscillators (FLO). Little is known about the distribution of homologs of the Neurospora clock proteins or about the molecular foundations of circadian rhythms across fungi. Here, we examined 64 diverse fungal proteomes for homologs of all five Neurospora clock proteins and retraced their evolutionary history. The FRH and FWD-1 proteins were likely present in the fungal ancestor. WC-1 and WC-2 homologs are absent from the early diverging chytrids and Microsporidia but are present in all other major clades. In contrast to the deep origins of these four clock proteins FRQ homologs are taxonomically restricted within Sordariomycetes, Leotiomycetes and Dothideomycetes. The large number of FRH and FWD-1 homologs identified and their lack of concordance with the fungal species phylogeny indicate that they likely underwent multiple rounds of duplications and losses. In contrast, the FRQ, WC-1 and WC-2 proteins exhibit relatively few duplications and losses. A notable exception is the 10 FRQ-like proteins in Fusarium oxysporum, which resulted from nine duplication events. Our results suggest that the machinery required for FWO oscillator function is taxonomically restricted within Ascomycetes. Although the WC proteins are widely distributed, the functional diversity of the few non-Neurospora circadian oscillators suggests that a WC-FLO oscillator is unlikely to fully explain the observed rhythms. The contrast between the diversity of circadian oscillators and the conservation of most of their machinery is likely best explained by considering the centrality of noncircadian functions in which RNA helicase (FRH), F-box (FWD-1), WC-1 and WC-2 (light-sensing) proteins participate in fungi and eukaryotes.