Cyanobacteria are commonly used for the phytostimulation and biofertilization of agriculture crops due to their nitrogen-fixing ability. However, the contribution by their phytohormones has been neglected. This study focuses on the screening of rhizospheric and free-living cyanobacteria for in vitro phytohormones production and growth stimulation in wheat. Selected isolates were shown to release cytokinin and indole-3-acetic acid (IAA) by using UPLC coupled with MS/MS via an electrospray interface. The maximum cytokinin and IAA concentration was 22.7 pmol mg−1 ch-a and 38 pmol mg−1 ch-a, respectively, in the culture medium of Chroococcidiopsis sp. Ck4 and Anabaena sp. Ck1. The growth of wheat inoculated with cyanobacterial strains was stimulated under axenic as well as field conditions. Seed germination, shoot length, tillering, number of lateral roots, spike length, and grain weight were significantly enhanced in inoculated plants. The maximum increase in grain weight (43%) was demonstrated in wheat plants inoculated with Chroococcidiopsis sp. Ck4 under natural conditions. Positive linear correlation of cyanobacterial cytokinin with shoot length (r = 0.608; P = 0.01), spike length (r = 0.682; P = 0.01), and grain weight (r = 0.0.869; P = 0.01) was recorded. Similarly, cyanobacterial IAA was correlated with the root growth parameters shoot length (r = 0.588; P = 0.01), spike length (r = 0.0.689; P = 0.01), and weight of seeds (r = 0.480; P = 0.05). The endogenous phytohormones pool of the plant was enhanced significantly as a result of the plant–cyanobacteria association in the rhizosphere. It was concluded that cyanobacterial phytohormones are a major tool for improved growth and yield in wheat.