Auxin (IAA) is an important regulator of plant development and root differentiation. Although recent studies indicate that salicylic acid (SA) may also be important in this context by interfering with IAA signaling, comparatively little is known about its impact on the plant’s physiology, metabolism, and growth characteristics. Using carbon-11, a short-lived radioisotope (t 1/2 = 20.4 min) administered as 11CO2 to maize plants (B73), we measured changes in these functions using SA and IAA treatments. IAA application decreased total root biomass, though it increased lateral root growth at the expense of primary root elongation. IAA-mediated inhibition of root growth was correlated with decreased 11CO2 fixation, photosystem II (PSII) efficiency, and total leaf carbon export of 11C-photoassimilates and their allocation belowground. Furthermore, IAA application increased leaf starch content. On the other hand, SA application increased total root biomass, 11CO2 fixation, PSII efficiency, and leaf carbon export of 11C-photoassimilates, but it decreased leaf starch content. IAA and SA induction patterns were also examined after root-herbivore attack by Diabrotica virgifera to place possible hormone crosstalk into a realistic environmental context. We found that 4 days after infestation, IAA was induced in the midzone and root tip, whereas SA was induced only in the upper proximal zone of damaged roots. We conclude that antagonistic crosstalk exists between IAA and SA which can affect the development of maize plants, particularly through alteration of the root system’s architecture, and we propose that the integration of both signals may shape the plant’s response to environmental stress.