Makwala paid tribute to a London Stadium crowd that defied incessant rain to cheer him on, seemingly louder than for Briton Nethaneel Mitchell-Blake, who finished third in their semi-final and also reached the final.
The day had started with Makwala crying foul about his treatment from the IAAF, the sport's governing body, after being barred from Tuesday's 400m final on medical grounds amid fears that he had fallen victim to the norovirus outbreak at the team hotel.
Injuries soon forced him to abandon the shorter sprints and take up the longer, more grueling 400m. I wish to thank the IAAF for giving me another chance and the crowd is so incredible.
But now Makwala will get the chance to face Van Niekerk later tonight.
"I am heartbroken", said the 30-year-old. "I feel this has been a waste of money and training".
"It's only because I'm not a Great British athlete".
"I'm still learning how to run the 200m and how to navigate the curve, but it's all learning and experience for the future".
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The IAAF has insisted it gave clear communication to the Botswana delegation that Makwala would not be allowed to run following a medical examination.
Olympic champion Faith Kipyegon of Kenya turned her 1500m silver at Beijing two years ago to a gold medal as the 23-year-old pulled away in the last 50 meters to clock 4:02.59 to win.
Bahamian Steven Gardiner claimed second, while Qatar's Abdalelah Haroun claimed the bronze.
Van Niekerk's bid for a first world double since 1995 now turns to the 200m, in which neither Usain Bolt nor the world's fastest man this season, Makwala, are running.
Nine people were still being affected, according to the IAAF.
Van Niekerk has an exhausting six races in six days across the 200m and 400m, as he aims to break two world records and win two gold medals at the World Championships.
"My whole year has been focused on the world championships", he said.
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There was a second world title for the Czech Republic's women's javelin world record holder Barbora Spotakova.
The only man likely to stop Makwala from winning gold now is Wayde van Nierkerk, the South African who won that 400m and is now looking to complete a track double. "The conspiracy theories will come out of the silence".
The race was a flat and one-sided contest, with van Niekerk barely celebrating his victory, instead easing up a full 15m from the line.
Speaking to the BBC, Makwala said that he believed star athletes such as Farah and Bolt would not have been treated in the same way by the IAAF. "It's such a massive pity". We only had benefit from the media relating to Makwala's not being allowed to compete which left us heart-broken. I've got so much sympathy.
"After I saw him cross the line on Tuesday I was like, this was my time".
However, IAAF president Sebastian Coe, writing in Wednesday's Evening Standard, said he sympathised with him but ultimately the IAAF's primary concern was for all the athletes and their health.
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