The European Commission vice-president was speaking in Athens where he was picking up an an honorary doctorate.
His acceptance speech, which heavily referenced classical Greece, came as the EU struggles with Brexit, Catalonia, tension among Eastern European member states and a rise of populist parties across the bloc.
And he warned his audience nothing is irreversible.
He said: “History should be our teacher, help us avoid mistakes of the past, make better choices for the future.
“But history should never become our master, choking us from behind and preventing us from seeing the path to the future with clarity.
“Nor should history become our slave, to be mishandled and to be sent out to do our dirty work when we look for an excuse for the next round of confrontation with our neighbours or other perceived rivals.”
Mr Timmermans said Europe reached its highest levels cultural, economic, technological and moral development when its governance was “based on the inalienable rights of individuals, enshrined in the rule of law, created by democracy”.
But he warned: “At the same time there is another powerful lesson here.
“Even the most successful system is never self sustaining and never invulnerable.
“After centuries of democracy, centuries of autocracy can follow.
“If you are not vigilant, do not adapt to new circumstances, lose the urge to ‘learn it all’ and fall into the trap of ‘knowing it all’, you might lose it all.
“The example of classical Greece shows clearly the in history regression is possible.
“It also shows that the fear for regression can push you into making the most horrible choices that aggravate rather that help the situation.”
The Commission president said the EU had much to do and faced many daunting challenges.
He said: “Resting on our laurels would just hasten decline.
“But as classical Greece teaches us, European efflorescence will remain possible for centuries to come if we retain our openness, curiosity, dissatisfaction with the way things are and willingness to make things better in cooperation with all those who share our values.”