Now, at the age of 32, it is the Monaco striker's chance to shine.
The question is: can the Colombia captain shoulder the huge burden of relaunching Los Cafeteros (the Coffee Makers) following a shock 2-1 defeat to Japan that has made their final Group H games against Poland and Senegal must-win encounters?
Colombia face Poland in Kazan on Sunday, when a second defeat for Jose Pekerman's technically-gifted side would spell national disaster.
"Today, we are in a situation in which we are forced to win. And we must do everything possible to win," Falcao said at Colombia's training base in Sviyazhsk just outside Kazan.
"We are now facing two teams who need to win, so for us these games will be like finals. It's them or us."
Cruelly deprived of competing in Brazil by a horrific knee injury, Falcao watched from the sidelines as James, whose sumptuous volley against Uruguay was voted goal of the tournament, took Colombia on a whirlwind journey on their first World Cup appearance since France '98.
Four years on and having relaunched his career with Monaco following a disastrous spell in England with Manchester United and Chelsea, Falcao has the chance to showcase the predatory talents that steered Atletico Madrid to the Europa League and Spanish Super Cup victories in 2012.
Falcao scored over 30 goals for Monaco in the 2016-2017 season to help steer the Principality club to the Champions League semi-finals and the Ligue 1 title, in front of Paris Saint-Germain.
Yet Colombia's inauspicious start has handed the Sainta Marta native a far bigger challenge than simply making amends for his absence in Brazil.
Despite Falcao and 10-man Colombia's best efforts, Yuya Osako's 73rd-minute winner sealed Japan's first win over a South American country, and exacted revenge for their 4-1 thumping by Colombia four years ago.
With James still doubtful, Pekerman is poring over the tactics required to both get the best out of Falcao and beat a Poland side that, following their 2-1 loss to Senegal, will be intent on adding to Colombia's woes.
Falcao, Colombia's all-time top scorer with 29 goals in 74 appearances, has highlighted the danger of Bayern Munich's Robert Lewandowski, calling him "a striker who can settle matches any time".
He also praised his Monaco teammate, no-nonsense central defender Kamil Glik, who is expected to return from a left shoulder sprain to shore up a Polish defence that was dangerously shaky against Senegal.
Poland defender Bartosz Bereszynski warned: "We know very well what is this game about, but we are optimists.
"One thing I am sure about is that we will not lack heart on Sunday."
Neither should Falcao, who is known throughout Colombia as 'El Tigre' (The Tiger).
"We've already put the Japan match behind us," he said.
"The simple fact we're still in contention at the World Cup gives us the emotional drive we need for these two games we have remaining."