Later in the day, Kenyan-born Bahraini Rose Chelimo won the women’s marathon after the more experienced Edna Kiplagat cracked over the closing stages to hand her the title in two hours 27 minutes 11 seconds.
Kirui, victor at the Boston Marathon in April, broke Tola, the fastest man in the field, with five miles (8.05km) of the 26.2-mile course left after they had gone head-to-head over the second half of the race.
At the 19-mile mark, Tola, the fastest man in the field, had made his decisive effort and sped away from the 24-year-old Kenyan but within two miles Kirui had hauled back the lead before surging away immediately and emphatically.
Kirui forged on so powerfully that by the end of the race as he came towards the line at Tower Bridge, he even had time to tap the hands of some of the hundreds of fans lining the finish.
“This is the best moment of my career, easily. I am so happy to win the world title because it is my first time at these championships,” Kirui said afterwards.
“This was the best course and the best crowd I have seen at a marathon.”
Kenya’s fifth men’s world champion at the distance eventually clocked 2 hours 8 minutes 27 seconds, finishing one minute and 22 seconds ahead of Tola (2:09:49).
The Ethiopian, who had tired rapidly after Kirui’s second wind, just held on for silver by two seconds from the fast-finishing Alphonce Simbu, who won Tanzania’s second medal ever at a World Championships.
Britain’s Callum Hawkins then earned the biggest cheers from the big crowds lining the streets when he came home in a remarkable fourth place in a lifetime best 2:10:17 amid familiar African domination.
In the women’s race, Chelimo led after 35km but defending champion Kiplagat overtook her before she regained her composure to win in two hours 27 minutes 11 seconds.
American Amy Cragg made a tremendous final burst to overhaul another Kenyan Flomena Daniel, who had looked set for the bronze medal.
Cragg also closed in swiftly on the tiring 37-year-old Kiplagat but had to settle for third place in the same time of 2:27:18.
“I had resigned and was happy with second position, but it was my day, my luck which handed me the title. It is not revenge even after she beat me in Boston. It was just my day. That is how running goes,” Chelimo told reporters.
“I wasn’t expecting to win the race although I enjoyed the race very much. After 35km, I pushed the pace, knowing Edna is a very strong and experienced athlete. But when I saw her overtaking me, I was happy to finish second,” she said.
The 37-year-old Kiplagat, who has won two world titles and two London Marathons and beat Chelimo to claim victory in Boston this year, was clear favourite but played down what is becoming a major rivalry.
“I trained well, but Rose was much stronger today. That is normal in running, you win today and lose tomorrow. It was Rose’s day today. I thought I trained well, but she was prepared better,” Kiplagat said.
“I know people put their bet on me, but at championships such things are normal,” she said.
“It was all fine until the 40km mark when my body gave in, I could no longer push. I am happy with this position, I spoke to my family who could not come and watch me due to delayed visa,” she said.