For a short period of time earlier this decade all marques were represented under the umbrella of the Formula One Teams' Association, with the common primary goal of trying to reduce costs.
But unable to agree on what became known as the 'resource restriction agreement', Red Bull and Ferrari pulled out of FOTA, followed by Toro Rosso and Sauber, leaving seven member teams at present.
With new engine regulations due to come into force from next season as F1 switches from 2.4-litre V8s to 1.6-litre turbo-charged power units, costs are currently spiralling out of control.
The lack of unanimity among teams has hamstrung efforts to keep a lid on spending and F1 supremo Bernie Ecclestone and Donald Mackenzie, co-founder of F1's majority shareholder CVC Capital Partners, both recently stated it is the teams' fault that the sport is so expensive.
In response to those comments, Whitmarsh, who is also chief executive of McLaren Racing, told Press Association Sport: "They have a point. The teams have to live in the commercial reality of the monies available.
"At the moment teams haven't controlled their costs enough, which is a never-ending project.
"Most healthy businesses are trying to control costs and maximise revenue, and in my view we're not doing a good enough job with both of those things.
"Any team not making a profit is spending too much money, which is a fundamental business error and not very sustainable.
"We can certainly do a better job if we work together rather than lobbing bricks at each other, which is sometimes what we end up doing.
"Undoubtedly we could work better together and say 'right, how do we make it even better than this?'
"So rather than talk about how it is spiralling down, how do we go out there and make this a dynamic and even more successful sport?
"As I say, we're not actively working together, and that's a shame."
Whitmarsh feels there are enough positives to guarantee continued long-term success for F1 rather than the constant scepticism surrounding the financial difficulties being faced by the teams.
"We have this culture in F1 where we're pretty good at being negative and we home in on the deficiencies," he added.
"If we're honest about it, and you stand back, there are positives.
"Primarily we've a fantastic sport which has huge potential. Bernie has done a fantastic job over the years to commercialise Formula One.
"We put on a great show, audiences are good, we're moving to relevant technologies, there are new sponsors coming in after what has been a difficult time, so the future looks more positive in that regard.
"There is a lot of good work being done, but we all know if we work together - with all the other partners in Formula One - we can make it even more successful.
"We're a multi-billion dollar entertainment business that needs to go out there and work harder."