The 32-year-old No. 8, who missed the first two games following surgery to drain a haematoma on his calf, is one of five changes to the starting XV who scraped a 23-18 win over Canada last weekend.
Parisse's aura is such that the Irish have said they fear the impact he could have on reviving his side's morale as they drive for a victory needed to maintain any hope of reaching the quarter-finals.
Parisse comes into the team for Samuela Vunisa and takes captaincy duties back from Leonardo Ghiraldini, who misses the match with a thigh muscle injury.
Parisse, who becomes the sixth Italy player to participate in four World Cups, is joined in the back row by Simon Favaro with whom he has formed a potent partnership.
Italy have won three of the last four tests when Parisse and Favaro started together in the back row, a sequence that began with Italy's first ever Six Nations win over Ireland, 22-15 in Rome in 2013.
That was prior to present Ireland coach Joe Schmidt taking over and guiding the Irish to two successive Six Nations titles (2014/15).
There are 13 players in Italy's match-day squad that were involved that day.
Aside from Parisse and Favaro three of them come in the pack, tighthead Lorenzo Cittadini, and locks Quintin Geldenhuys and Josh Furno.
A win for Ireland at the Olympic Stadium on Sunday would see both them and France qualify out of Pool D for the knockout stages.