Inexperienced Bairstow struggled at number six in the three-Test home series victory against West Indies in May and June with the short ball especially causing him problems.
Bopara, who can also bowl medium pace, has rarely looked convincing during his 12 Test appearances but shone with the bat in the recent limited overs matches against West Indies and Australia.
The rest of the squad for the Oval Test in London is as expected with fast bowlers James Anderson and Stuart Broad recalled having been rested for the final rain-hit Test against West Indies.
“Ravi Bopara has worked hard to regain his place in the Test squad following some injury concerns earlier in the season and is the only player included who is yet to play a Test match this summer,” England selector Geoff Miller said in a statement on Sunday.
“We know we will need to play excellent cricket to win this three-match series and the squad will be determined to start with a strong performance this week during the first Test and set the tone for the rest of the series.”
England, the top-ranked Test side, will be surpassed by South Africa if the Proteas win the series.