Terry called time on his England career in 2012, accusing the Football Association of making his position within the international set-up "untenable" following its pursuit of a racism charge against him.
After being part of a team that conceded just four goals in qualifying, Jagielka has every right to feel annoyed every time someone insists Terry should have been coaxed out of retirement.
"It's difficult. I can't say I particularly like to hear it," Jagielka said when asked about calls for Terry's return.
"I understand why I do (hear it). Obviously Gaz and JT play together at Chelsea, they play in the Champions League and were contenders to win the Premier League.
"I was asked the other day, that while our attack looks good would our defence be okay? I felt like laughing.
"Our defensive record in the qualifiers was pretty decent, but I can't stop what people are going to ask. I stop, smile and get on with it."
He may be fresh-faced and lean after an intense week-long training camp in Portugal, but make no mistake - Jagielka is very much a senior member of this England squad.
At 31 years old, he knows this will probably be his last chance to play on the biggest stage in world football and is determined to make the most of it.
"My career path has been slightly different to some of the lads who have been involved with England since they were teenagers," said Jagielka, who was an unused substitute during Euro 2012.
"If I had got a chance I would have tried to seize the moment at the Euros, but it wasn't to be.
"Hopefully I will this time. I know at 31 I won't be around forever and this could be my one tournament."
Cahill and Jagielka first played together in England's 1-1 draw with Ghana in 2011 yet their paths almost crossed four years earlier.
In their 10 appearances together for the national side, they are yet to taste defeat and eight goals have been conceded.
Cahill, who hails from Dronfield just outside of Sheffield, shares a common interest in the Steel City with Jagielka which has helped them develop a close relationship.
"He is a Sheffield lad and I played for them so there is plenty to talk about," Jagielka said.
"Our relationship is a good one. We spend a lot of time together and we laugh and joke.
"We do not have a tremendous amount of caps but they have mostly been with each other."
Although England are big outsiders - one bookmaker is offering 100-1 on the Three Lions going all the way in Brazil - there is a cautiously optimistic feel around the camp after a trouble-free training camp in Portugal.
"The squad is quite a young squad and there are not too many skeletons to come out of the closet!" Jagielka said.
Jagielka rejects the idea that England are miles behind their European counterparts in terms of producing exciting young talent.
The centre-back says Liverpool's Raheem Sterling has had a better year than Gerard Deulofeu, the 20-year-old who has been called up to the Spain squad after spending the season on loan at Goodison Park.
Jagielka also uses the emergence of Everton team-mate Ross Barkley, who has made the 23 despite having just three caps, as a reason for optimism.
"I knew Ross was something special from the age of 14," Jagielka added.
"People compare him to Wayne (Rooney). They are not the same players but in terms of mindset, they are."
- Sports & Recreation
- Gary Cahill