In 2021/22 the force forked out £542,000 of taxpayers' cash on officers for games at Molineux and Villa Park, according to data from a Freedom of Information request.
Clubs are only required to pay for policing on their "footprint", such as inside the ground and on club car parks. It means the cost of police patrolling nearby streets and at sites such as railway stations is taken from the public purse.
West Midlands Police and Crime Commissioner (PCC) Simon Foster said while the force had a duty to make sure fans felt safe, it "expects to cover its costs" over the course of a season.
Last season almost £280,000 was spent on police at Villa, while the Wolves bill was £262,000.
Villa saw 27 arrests across the season, while Wolves had 20. The figures include one man who was arrested when violence erupted at Wolverhampton railway station after the two clubs clashed at Molineux in April.
There were four arrests for possession of cocaine at the two grounds last season, one at Villa Park and three at Molineux.
PCC Mr Foster said: "Football deployments are made in line with individual contracts with each club. All are based on agreed threat and risk analysis that categorises each fixture.
"The Ipswich ruling found that police forces can charge football clubs only for officers deployed on the stadium footprint – inside the ground and in the immediate area around it.
"Of course in reality officers also have to police approaches to the stadium and transport hubs on certain matchdays too. It is only right that supporters expect to feel safe on their way to and from stadiums.
"Over the course of the season, West Midlands Police expects to cover its costs."
In a landmark case in 2017 Ipswich Town successfully argued that the club should not have to pay for policing on streets leading up to their ground.
According to West Midlands Police, the number of officers on duty can vary from single figures to several hundred, depending on the opposition and the expected crowd size.
In the Championship, the force spent £93,000 policing Blues home games in 2021/22. A total of 34 arrests were made.