The tournament has traditionally been held in January and February, with the timing of the tournament a source of frustration to European clubs forced to release players in the middle of the season.
The CAF executive committee confirmed the changes to the format following a two-day symposium in Rabat, although the tournament will continue to be held every two years and exclusively on African soil.
The decision to increase the number of teams mirrors a similar one taken by UEFA to expand the European Championship, with 24 nations taking part at Euro 2016 in France.
The advantage would be more teams exposed to top-level competition and the disadvantage a dilution of the qualifying competition with virtually one in every two teams qualifying.
The expansion of the African competition could also reduce the number of countries capable of staging the event, with 2019 hosts Cameroon already behind schedule and facing the prospect of having to pull out.
Algeria and Morocco, who were disqualified from the 2015 edition after refusing to host it due to fears about the Ebola virus, would reportedly be interested in taking over.
With at least six stadiums needed instead of four, another option would be to permit multiple countries to co-host the tournament.
Madagascar's Ahmad Ahmad scored a shock CAF presidential triumph over long-serving Cameroonian Issa Hayatou in March and vowed to thoroughly review African football.
Hayatou consistently rejected suggestions of a move to June, saying the weather then was too hot in northern Africa, too wet in the west and centre and too cold in the south.
But his view was as much about not bowing to pressure from Europe as climatic conditions because African national teams and clubs play regularly during June without adverse effects.
The decision taken by several players to turn down call-ups for their national team has swayed Ahmad's mind toward change.
Liverpool defender Joel Matip was one of seven Cameroon players who refused to be considered for selection, saying their club careers were more important than national duty.
Cameroon remarkably still went on to win the tournament as they beat Egypt 2-1 in the final, lifting the trophy for a fifth time.
Qualifying for the 2019 edition is already underway, with 48 teams competing across 12 groups for a place at the finals.