Justin Fashanu became the first openly gay footballer in 1990, but very few others have followed suit since then.
United States international Robbie Rogers came out in 2013, while former Aston Villa and Everton midfielder Thomas Hitzlsperger announced he was gay the following year after hanging up his boots.
Scudamore, however, would welcome an active player in the game breaking through the barrier, believing they would be accepted for who they are.
"The environment would be entirely suitable for them to come out," Scudamore told the BBC's Newsnight show.
"It would be welcomed and I think there would be a tolerance to it. I think the time would be right to do that."
In the interview, Scudamore admitted he is certain there are gay players currently in action in the Premier League.
"It would be very strange if there wasn't," he added.