A key member of Wales' squad for the World Cup and their Grand Slam-winning Six Nations, Priestland came under fire during the 3-0 defeat to Australia in the summer.
However Howley insists that the fly-half needs to be treated with care having only become first choice for Wales in the last year.
Howley told walesonline: "Rhys has played a huge part in what Wales have achieved over the last 12 months.
"Everyone knows about his performances at the World Cup and he was exceptional in the second half of the Grand Slam game against France in terms of playing territory.
"Rhys knows in certain components of his game he wasn't at his best in Australia and that overall his play wasn't to the standard he achieved in the World Cup.
"But he has only been playing at ten for Wales for ten months
"You talk to Neil Jenkins about the criticism he had over a decade of playing there.
"Number ten has always been a big focus in Wales and that will never change.
"Our overriding opinion throughout the Test series was that Rhys was our number one fly-half. And I still believe that to be the case.
"There are always going to be challenges for Rhys moving forward in his game.
"It will be interesting to watch the couple of months in September, October going into the autumn series.
"But, to my mind, he is still our number one fly-half."
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