South Africa's Motsepe elected president of CAF
"Africa needs collective wisdom, but also the exceptional talent and wisdom of every (national football association) president and every member nation," he said.
"When we all work together, football in Africa will experience success and growth that it has not enjoyed in the past."
Africa has suffered serious setbacks in recent years with all five qualifiers for the 2018 World Cup in Russia eliminated after the first round -- the continent's worst showing in 36 years.
Last November, Malagasy Ahmad Ahmad became the first CAF president to be banned by FIFA, with a five-year suspension for "governance issues" cut to two after appealing to the Court of Arbitration for Sport.
Just a few weeks ago, Motsepe, Ivorian Jacques Anouma, Mauritanian Ahmed Yahya and Senegalese Augustin Senghor were locked in an intriguing struggle for the presidency.
But FIFA-brokered meetings of the contenders in Morocco and Mauritania led to mining magnate Motsepe becoming the sole candidate. Senghor and Yahya were given the first and second vice-president roles.
Anouma, who initially declared the pact "undemocratic", is a former FIFA executive committee member and becomes a special advisor to Motsepe.
As some CAF officials railed against alleged interference by the world body, FIFA president Gianni Infantino played down the role of his organisation.
"I am delighted that FIFA has been able to contribute, even if just a little, to this crucial moment for football on this great continent," he said.
- 'Stop the massacre' -
Former Africa Cup of Nations-winning coach Claude le Roy questioned the involvement of FIFA in Motsepe's election, given they "would not dare do so in Europe or South America".
"Infantino, stop the massacre with African football ... imposing your law on Africa in the elections," Le Roy told AFP.
It is not the first time FIFA has been accused of interfering in CAF with many officials believing Infantino privately backed Ahmad four years ago.
The Malagasy ended the 29-year reign of Cameroonian Issa Hayatou in a shock outcome to the 2017 presidential election.
But after a promising start, Ahmad stumbled from one crisis to another, which eventually led to him exiting the presidency in disgrace.
FIFA became so concerned by governance issues at CAF that it sent FIFA secretary general Fatma Samoura to Cairo for six months to assist in the running of the confederation.
Motsepe is the ninth richest man in Africa with a personal wealth estimated at $2.9 billion (2.4 billion euros) by Forbes magazine. He owns 2016 CAF Champions League winners Mamelodi Sundowns.
He inherits an organisation described as a "cesspool of corruption and self interest" by South African newspaper the Daily Maverick.
"CAF desperately needs to break from its tired old ways, institutionalised habits and the sense it serves those who sit on its executive committee, rather than the other way round," wrote the publication.
"More importantly, it needs to find more revenue streams and must dramatically improve the quality of its products to do so."
CAF are banking on Motsepe, a fan of Spanish giants Barcelona, using his business connections across Africa to woo new sponsors.
France-based oil and gas giant Total are the main financial backers, but details of the eight-year deal that began in 2016 have never been disclosed.