Mr Ackermann said that Mr Wauthier's family believed he was partly to blame for the tragedy.
The Swiss insurer's board said it had accepted his decision "with deep regret". Vice-chairman Tom de Swaan will take his place.
Mr Wauthier was found dead at his home on Monday.
Mr Ackermann, a former chief executive of Deutsche Bank, said on Thursday in a statement: "The unexpected death of Pierre Wauthier has deeply shocked me.
"I have reasons to believe that the family is of the opinion that I should take my share of responsibility, as unfounded as any allegations might be."
He added that he was stepping down "to avoid any damage to Zurich's reputation".
Zurich Insurance company employs about 60,000 people in 170 countries.
Mr Wauthier, aged 53, was a British and French citizen and joined the company 17 years ago. Before that, he worked for US bank JP Morgan.
This is the second recent high-profile corporate death in Switzerland, after last month's suicide of Swisscom's 49-year old chief executive Carsten Schloter.
Zurich Insurance's chairman Josef Ackermann has resigned, three days after the apparent suicide of its chief financial officer Pierre Wauthier.