World champion Lewis Hamilton and many of Bianchi's pitlane colleagues joined family and friends of the talented young Marussia driver who died in Nice on Friday, nine months after his devastating accident at the Japanese Grand Prix.
Two giant portraits of Bianchi in full racing gear adorned the walls either side of the cathedral's main entrance.
His coffin, with his No 17 helmet resting on it, was carried from the hearse into the cathedral by a group of young drivers, described by Father Sylvain Brison as Bianchi's "racing brothers".
With The Eagles' haunting 1970s anthem "Hotel California" playing in the background, the coffin was carried up the cathedral's central aisle.
Hamilton and his Mercedes teammate Nico Rosberg, who had made the short trip from their homes in Monaco, as well as Jean Todt, head of F1's governing body, the FIA, and the French Sports Minister Thierry Braillard, were in attendance for what Bianchi's parents had requested was to be an intimate farewell to their son.
"Jules' death is deeply unjust," Father Brison told the mourners in the Sainte-Reparate Cathedral situated in Nice's historic old town.
"He was happy, because he had turned his dream into reality."
F1 "was his life, his vocation. He was a champion blessed with a rare talent, as well as being a young man whose stature was as high as the depth of his humility".
He concluded the service by saying: "Jules never managed to make it on to the Formula One podium, and so I ask you to applaud him now," which the emotional gathering, both inside and outside the cathedral, duly did for several minutes.
The service ended with the playing of the tender 1980s classic hit "Mistral Gagnant" by French singer Renaud.