Brassinosteroid signaling is essential for plant growth as exemplified by the dwarf phenotype of loss-of-function mutants in BRASSINOSTEROID INSENSITIVE 1 (BRI1), a ubiquitously expressed Arabidopsis brassinosteroid receptor gene. Complementation of brassinosteroid-blind receptor mutants by BRI1 expression with various tissue-specific promoters implied that local brassinosteroid signaling may instruct growth non-cell autonomously. Here, we performed such rescues with a panel of receptor variants and promoters, in combination with tissue-specific transgene knockouts. Our experiments demonstrate that brassinosteroid receptor expression in several tissues is necessary but not sufficient for rescue. Moreover, complementation with tissue-specific promoters requires the genuine BRI1 gene body sequence, which confers ubiquitous expression of trace receptor amounts that are sufficient to promote brassinosteroid-dependent root growth. Our data, therefore, argue for a largely cell-autonomous action of brassinosteroid receptors.