Abstract Tendon injuries are common and often heal poorly. While developing tendons heal without scarring, this capacity declines with age, yet the underlying cellular transitions remain poorly defined. Here, we integrate histological, single-nucleus, single-cell, and spatial transcriptomic profiling of human Achilles and quadriceps tendons across embryonic, foetal, and adult stages, including ruptured adult tendons. We identify seven embryonic progenitor states that give rise to three distinct tendon-associated fibrillar, connective tissue, and chondrogenic lineages. These populations diversify during development and occupy distinct spatial niches, adopting specialised roles in matrix synthesis, tissue remodelling, and mechanical adaptation. While non-fibroblast populations remain transcriptionally stable with age, fibroblasts undergo marked reprogramming, shifting to homeostatic or injury-responsive states. In ruptured adult tendons, a subset of fibroblasts partially reactivates developmental programs but remains transcriptionally distinct from their regenerative counterparts. These findings define the cellular architecture of human tendon development and ageing and reveal lineage-specific targets for therapeutic repair. Data description This dataset comprises the 10X Visium spatial transcriptomics data from human fetal Achilles (Dev16126_Ach_EnthMB) and Quadriceps (Dev16126_Quad_MB and Dev16126_Quad_MB2) tendons. For each sample this dataset contains: cellranger filtered_feature_bc_matrix spatial files, including Loupe files Methods: Foetal Achilles (N=1) and quadriceps tendons (N=2) (Table S1) were dissected from both legs of a single 20 pcw foetus and flash frozen in liquid nitrogen. In preparation for spatial transcriptomics (ST), the samples were cut to ≤0.65 cm² to fit the 10x Genomics Visium ST slide regions. We were able to retain enthesis-to-MTJ as well as adjacent muscle tissue regions for both types of tendons. The samples were embedded in cold OCT mounting medium (VWR) on dry ice and cut longitudinally into 10 μm sections, which were then fixed and stained with H&E to verify tissue morphology and suitability. The sections were prepared for sequencing according to the 10X Genomics recommended protocols using the Visium Gene Expression Slide and Reagent Kit alongside a Dual Index Kit TT Set A. Libraries were sequenced using Illumina NextSeq500 (paired-end) at a depth of 54,000 (Quad2 tendon), 74,000 (Ach) and 119,000 (Quad1) mean reads per spot. The data and images were processed with SpaceRanger (v1.3.1; 10X Genomics) using default settings and mapped to the GRCh38 reference genome.