Khawaja opened a can of worms this week with the publication of his autobiography that revisits the 2018 ball-tampering scandal in South Africa that rattled Australian cricket.
He also revealed in the book that he was upset when overlooked to be captain after then-skipper Steve Smith was sent home from Cape Town. Tim Paine got the job instead and was succeeded by Cummins in 2021.
"I was a natural selection for interim captain, but was overlooked," said Khawaja, Australia's first Pakistan-born national player who was Queensland captain at the time.
He suggested it was because he had been a prominent protagonist during earlier pay disputes with Cricket Australia, but also due to his heritage.
"The second -– and, I believe, more important -– reason was that they weren't ready for a brown Australian cricket captain, even as an interim."
Cummins said he did not agree with Khawaja's rationale.
"I think of the things I've read, that's the most serious," Cummins said at a press conference to address the ball-tampering allegations reignited by Khawaja.
"To think that the job I hold is quarantined from people based on their skin colour, it's a pretty big statement. If you are going to say that I think you have to have evidence. And I just don't think that's the case.
"Again, I agree with Usman on a lot of things but I disagree with him saying that if you're Australian captain you have to be of a certain skin colour, I have to disagree with that statement."
The now-retired Khawaja, who immigrated as a child, has often spoken about the racism he faced from a young age, but has been reluctant to take any credit for opening doors.
Asked if he had seen conduct he considered racist since becoming Australian captain, Cummins said: "I'd rather not go into that. I think that's maybe a story for Uzzie.
"But nothing since I've been captain that I can think of."