Troy Brown's career in local government began in 1994, when he accepted a position as recreation specialist for Santa Clarita, California. He then moved up the ranks in the city, serving as an information technology specialist and then management analyst. He then joined Riverside, California, where he served as assistant to the city manager, and later as budget manager and assistant to the city manager in Elk Grove, California. Before joining Moorpark, he served as assistant city manager of Livermore, California and then as city manager of Tracy, California.  He became the city manager of Moorpark in 2018.

Brown has been an active member of ICMA (International City/County Manager Association) since 2004. He was elected by the membership in 2011 to serve a three-year term as West Coast Regional Vice President on the ICMA Executive Board. He then served as co-chair of the Task Force for Strengthening Inclusiveness in the Profession, and as an ICMA-appointed representative on the Vantage Trust Board of Directors, 2015-2017. Troy served as President of the ICMA in 2020-2021.