Ingebrigtsen will be pinning his hopes on there being no repeat of the last two world championship finals.
In Eugene in 2022 and then in Budapest last year, the Norwegian was beaten down the home stretch by Britons, respectively Jake Wightman and Kerr.
Wightman is out of the Olympics with an injury, leaving Kerr to have Ingebrigtsen in his crosshairs even though their head-to-head record in 1500m finals stands at 8-1 in favour of the Norwegian.
It was Kerr who beat Ingebrigtsen the last time they clashed in the mile at the Diamond League meeting in Eugene in May.
Since then, Ingebrigtsen has been unbeaten, winning the Diamond League 1500m on home soil in Oslo, European 1500m and 5000m titles in Rome, a Norwegian championships double, and that 1500m in Monaco.
"I think it's healthy for the event and the sport," Kerr said of his rivalry with the Norwegian.
"I don't mind about the rivalry. But this is my job, my job's to be out here and win medals. I am lucky that I have a chance to be here and compete. People are welcome to talk about it."
On Friday, Ingebrigtsen looked comfortable in finishing third in his heat won by Dutchman Stefan Nillessen in 3min 36.77sec.
Kerr showed a keen pair of heels to win his heat in 3:35.83 and will be joined by British teammate Neil Gourley in the semi-finals, but not George Mills, who has a second chance through Saturday's repechage.
"I just want to make sure I get though the rounds healthy, and then I'll be looking to keep the rhythm from there," Kerr said.
Ingebrigtsen comes into the Olympics in form having recently improved his own European record to 3:26.73sec in Monaco.
Ermias Girma of Ethiopia won the other heat in 3:35.21 with Kenya's 2019 world champion and Tokyo Olympics silver medallist Timothy Cheruiyot also going through.
World Athletics president Sebastian Coe said the 1500m had "added piquancy because this is probably not a friendship made in heaven".
"That doesn't bother me either. We know we want that kind of thing in the sport. So it really could be a race for the ages."
Should Ingebrigtsen claim back-to-back titles, he would be just the second man after Coe in 1980 and 1984 to win two Olympic 1500m golds.
Also qualifying from Friday's heats were American Yared Nuguse, Norway's world bronze medallist Narve Gilje Nordas and 19-year-old Niels Laros of the Netherlands, fresh from running a world under-20 1000m record of 2:14.37 in July.
The semi-finals are set for 1910 GMT on Sunday, with the final scheduled for Tuesday (1850 GMT).