Les Bleus made it two wins from two thanks to the right-back's header, though they rode their luck against a spirited Guinea side, who had two first-half goals disallowed.
Amadou Diawara forced Guillaume Restes into a superb fingertip save just minutes into the tie before Jean-Philippe Mateta wasted a hat-trick of chances to put the hosts ahead.
A cheeky backheel dribbled wide, and a thumping header missed the target on either side of Soumaila Sylla's smothering save.
Naby Keita clinically picked out the bottom corner from an offside position just before half-time, with Abdoulaye Toure also seeing a goal ruled out moments later after meeting a free-kick.
France came to life in the second half and gave a warning sign when Loic Bade struck the post from a tight angle.
In the end, Sildillia proved the difference as he was left unmarked to meet Michael Olise's cross, and Sylla could not get to his thumping header.
France are through to the next round, and top Group A with six points, while Guinea sit bottom of the group having lost both of their matches so far.
Data Debrief: Les Bleus leave it late
For much of the first half in this game, France were sluggish and could have easily gone into half-time 2-0 down if it was not for two tight offside calls.
In the end, Thierry Henry's side showed their quality, with Olise proving the key man. He created six chances, more than anyone else on the pitch, with one of those resulting in an assist.
It is the first time France have reached the quarter-finals at the Olympics since 1996, as they looked to end a 40-year wait for a gold medal in the event.
Thierry Henry's side remain the only side in the tournament to win all of their games so far, and made light work of their opponents on Tuesday.
Jean-Philippe Mateta, who captained the side with Alexandre Lacazette on the bench, started off the scoring after the ball bundled its way into his path before finishing beyond Alex Paulsen in the 19th minute.
In a game that saw Les Bleus accumulate 34 shots at the Orange Velodrome, their dominance was rewarded with two quickfire goals late on.
Desire Doue would double the hosts' advantage from close range, with Arnaud Kalimuendo rounding off the scoring three minutes later to see France remain perfect.
France's triumph saw them win their first three games at the Games for the first time in their history, while also keeping three clean sheets on the spin for the first time at the Olympics.
In the other Group A encounter, the United States qualified for the knockout stages of the tournament for the first time since 2000 as they eased to a 3-0 win over Guinea.
A rampant start to the encounter saw Djordje Mihailovic and Kevin Paredes have Marko Mitrovic's two goals to the good just after the half-hour mark.
Despite finishing the encounter with just 37.8% possession, the United States were clinical in the final third as Paredes put the game beyond doubt in the 75th minute.
They return to action this Friday when they face Group B winners Morocco, who clinched top spot with a 3-0 win over Iraq while also finishing ahead of Argentina.
Les Bleus were minutes away from a semi-final exit against the Pharaohs until Jean-Philippe Mateta's 83rd minute equaliser.
Mateta would grab his fourth of the tournament in the ninth minute of extra-time, with former Crystal Palace teammate Michael Olise confirming the 3-1 win soon after.
Henry had been preparing for this event since taking over in August 2023 and felt the weight of responsibility, having seen his nation perform brilliantly in other events as the hosts.
“I’m living a dream. I don’t want to wake up," Henry said.
"I’ll be honest with you, what’s nice is for Team France because when you see everyone winning medals here and there, you think it’s up to us not to let the guys down.”
Henry endured a torrid time in charge of Monaco over five years ago, winning five of his 20 games in charge (D4, L11), but has since rebuilt his career.
Firstly, in the MLS with Montreal Impact, leading Montreal to their first playoff berth in four seasons, before returning for a second stint with the Belgium national side as an assistant manager.
This tournament has seen Henry possibly stake a claim for the France job further down the line, with Didier Deschamps’ contract expiring after the 2026 World Cup.
However, Philippe Diallo, president of the French Football Federation, did not want to entertain the idea just yet.
Diallo told RMC: “Let’s not rush things. Thierry Henry, when I appointed him to the position, there were some who had doubts given what he had done previously. I had confidence in him and he is proving it.”
France will play Spain at the Parc des Princes on Friday in the showpiece final.
France last triumphed in the competition at the 1984 games in Los Angeles, failing to reach the knockout stages at the Tokyo Olympics back in 2020.
But under the guidance of Thierry Henry, who scored 51 goals for Les Bleus during his international career, the French are among the favourites to scoop the top honour.
Henry's side have won two of their three pre-tournament friendlies this month, the latest result ending in a 1-1 draw with Japan, who won bronze in the 1968 games.
Lacazette was named by Henry as the nation's captain ahead of the competition, and will lead Les Bleus' star-studded line-up out against the United States in Marseille on Wednesday.
Jean-Philippe Mateta, Michael Olise, Rayan Cherki and Manu Kone are just some of the names at Henry's disposal.
Having not featured for Didier Deschamps' side since 2017, Lacazette explained that the squad are in unison of achieving gold at their home games.
"We all have the same ambition, to go all the way and win a medal," the 33-year-old said. "The fact that it’s a home games is really going to motivate us."
Henry has lost just two of his 11 games in charge of France's U21 and U23 sides (W7, D2) since being appointed back in August 2023.
Former Arsenal forward Lacazette said Henry wanted the team to play an attacking, possession-based style of football heading into the tournament.
"Tactically, he is decidedly forward-thinking... he especially wants us to enjoy ourselves and put on a show for the spectators,” Lacazette said.
Following their Group A opener against the United States, France will play Guinea and New Zealand.
