Nightingales are renowned for their large song repertoire, including the acoustically distinct type of so-called whistle songs. These contain temporal sequences of unmodulated tonal syllables, known as whistle syllables, defining the fundamental frequency of the song, i.e., the pitch. While recent research has shown nightingales’ ability to adjust acoustic structure to match pitch, the flexibility of their temporal structure remains unexplored. Here, we show that nightingales exhibit a consistent rhythmic pattern in their whistle songs, with a shift in pitch distribution toward lower frequencies as tempo increases. We analyzed whistle songs of naturally singing nightingales and defined tempo as the temporal distance between the onset of whistle syllables. We found whistle songs had a consistent rhythms across a trimodal distribution of tempos, categorizing whistle songs’ tempi into fast (<250 ms), medium (250 - 500 ms), and slow (> 500 ms). Nightingales possess a broader pitch range at slower tempos, while higher tempos correlate with a shift towards lower frequencies. Next, we faithfully reconstructed whistle syllables’ temporal and spectral dynamics in a model that describes syringeal dynamics in songbirds, so as to validate the lack of underlying physical constraints of varied whistle syllable production. Finally, we conducted fieldwork to investigate spectral-temporal trade-offs in whistle songs. To this end, we generated synthetic whistle songs that challenge the nightingales’ matching capabilities. Preliminary results show that nightingales can adjust their responses to spectral, temporal or both features simultaneously, offering insights into the optimization strategy guiding their vocal behavior, confirming the results of our model.