Joining TxDOT's Travel and Information Division in 1979, Howdeshell worked in administration until 1984. Then she became assistant to the director of the Travel Services Section. Promoted to staff services officer for the division in 1985, Howdeshell became responsible for personnel, accounting, budgeting, purchasing, training, and material and property management. While deputy division director from 1992 to 1995, she also served as legislative liaison and interim division director prior to being selected as division director.

Howdeshell's management responsibilities include the "Don’t Mess with Texas" campaign to prevent litter. This program is considered one of the most successful of such initiatives. She is also responsible for the state’s Adopt-a-Highway volunteer program. This program has spread to 48 other states and several countries from its beginning in TxDOT’s Tyler District in 1985.

In promoting Texas as a premier tourist destination, Howdeshell coordinates with the Governor’s Office of Economic Development and Tourism, the Texas Commission on the Arts, the Texas Historical Commission, and the Texas Parks and Wildlife Department. Howdeshell serves on the Texas State Agency Tourism Council and is a past chairwoman. A primary state representative to the tourism industry, she also serves as an ex officio member of the Texas Travel Industry Association Board of Directors and has served as an Advisory Board Member of AAA Texas.