The club have responded to supporters, who are unhappy that there is no central ticket office in town after the last one closed down in May.
The new kiosks will be in the Transport Museum and the Tourist Information Centre in the Cathedral Ruins.
You will be able to buy tickets from these outlets from Wednesday.
Tickets will be available from Coventry Transport Museum from 10am to 4.30pm seven days a week.
Staff from the Cathedral Tourist Information Centre will also sell match tickets between 9.30am and 5pm from Monday to Friday and from 10am to 4.30pm on Saturdays and Sundays. The only exception is on the second and fourth Sunday each month when the shop is closed from noon to 1pm
Said Nathan Kosky: "We closed our shop in West Orchards Shopping Centre in June and since my arrival at the club in the summer, I have been aware that some fans find it difficult to travel to the Ricoh Arena to buy their tickets or don't have access to a computer to buy their tickets from our official website
"We have been searching for an alternative for some time and we think opening ticket booths at Coventry Transport Museum and the Tourist Information Centre will resolve the issue to everybody's satisfaction.
"This will give everybody the opportunity to buy tickets at their convenience whenever they are in the city centre. "The move also shows commercial sense because we are linking up with established outlets as well as improving our service to supporters.
"It is very important that the club has a presence in Coventry city centre and we're very excited about this partnership," said Nicola Leake from CV One who had been involved in setting up these offices.
"This is a fantastic opportunity for both the club and the Tourist Information Centre. "We are really glad to support CCFC and now have not one, but two ticket outlets based in the city centre. By working with the football club, we are able to make obtaining tickets to games more accessible for everyone. "