diff --git a/server/src/http/workflow/story_ops.rs b/server/src/http/workflow/story_ops.rs
index c9552acb..de277df3 100644
--- a/server/src/http/workflow/story_ops.rs
+++ b/server/src/http/workflow/story_ops.rs
@@ -264,11 +264,20 @@ pub fn add_criterion_to_file(
         }
     }
 
-    let insert_after = last_criterion_line
-        .or(ac_section_start)
-        .ok_or_else(|| format!("Story '{story_id}' has no '## Acceptance Criteria' section."))?;
-
     let mut new_lines: Vec<String> = lines.iter().map(|s| s.to_string()).collect();
+
+    let insert_after = if let Some(idx) = last_criterion_line.or(ac_section_start) {
+        idx
+    } else {
+        // No ## Acceptance Criteria section — create one on demand.
+        if new_lines.last().map(|l| !l.is_empty()).unwrap_or(false) {
+            new_lines.push(String::new());
+        }
+        new_lines.push("## Acceptance Criteria".to_string());
+        new_lines.push(String::new());
+        new_lines.len() - 1
+    };
+
     new_lines.insert(insert_after + 1, format!("- [ ] {criterion}"));
 
     let mut new_str = new_lines.join("\n");
@@ -353,6 +362,13 @@ pub fn update_story_in_file(
     let mut contents = read_story_content(project_root, story_id)?;
 
     if let Some(fields) = front_matter {
+        if fields.contains_key("acceptance_criteria") {
+            return Err(
+                "'acceptance_criteria' is a reserved field managed via the story body \
+                 (use add_criterion / remove_criterion / edit_criterion instead)."
+                    .to_string(),
+            );
+        }
         for (key, value) in fields {
             let yaml_value = json_value_to_yaml_scalar(value);
             contents = set_front_matter_field(&contents, key, &yaml_value);
@@ -612,7 +628,9 @@ mod tests {
     }
 
     #[test]
-    fn add_criterion_missing_section_returns_error() {
+    fn add_criterion_creates_section_when_missing() {
+        // Bug 625: adding a criterion to a story that has no ## Acceptance Criteria
+        // section (e.g. a spike converted to a story) must auto-create the section.
         let tmp = tempfile::tempdir().unwrap();
         setup_story_in_fs(
             tmp.path(),
@@ -621,8 +639,92 @@ mod tests {
         );
 
         let result = add_criterion_to_file(tmp.path(), "12_test", "X");
-        assert!(result.is_err());
-        assert!(result.unwrap_err().contains("Acceptance Criteria"));
+        assert!(
+            result.is_ok(),
+            "should succeed by creating the section: {result:?}"
+        );
+
+        let contents = read_story_content(tmp.path(), "12_test").unwrap();
+        assert!(
+            contents.contains("## Acceptance Criteria"),
+            "section should be created"
+        );
+        assert!(contents.contains("- [ ] X"), "criterion should be present");
+    }
+
+    /// Bug 625: spike-to-story conversion + AC addition end-to-end.
+    ///
+    /// Simulates: create spike content (no AC section), convert to story via
+    /// update_story front_matter type field, then add_criterion three times,
+    /// and assert all three appear in the AC section.
+    #[test]
+    fn spike_converted_to_story_accepts_add_criterion() {
+        let tmp = tempfile::tempdir().unwrap();
+
+        // Spike content: no ## Acceptance Criteria section.
+        let spike_content = "---\nname: \"My Spike\"\n---\n\n\
+                             ## Question\n\n- What is the best approach?\n\n\
+                             ## Hypothesis\n\n- TBD\n\n\
+                             ## Findings\n\n- TBD\n\n\
+                             ## Recommendation\n\n- TBD\n";
+        setup_story_in_fs(tmp.path(), "100_spike_my_spike", spike_content);
+
+        // Convert spike to story by updating the type field.
+        let mut fields = HashMap::new();
+        fields.insert("type".to_string(), Value::String("story".to_string()));
+        update_story_in_file(tmp.path(), "100_spike_my_spike", None, None, Some(&fields))
+            .expect("converting spike type to story should succeed");
+
+        // Add three acceptance criteria.
+        add_criterion_to_file(tmp.path(), "100_spike_my_spike", "First criterion")
+            .expect("add first criterion");
+        add_criterion_to_file(tmp.path(), "100_spike_my_spike", "Second criterion")
+            .expect("add second criterion");
+        add_criterion_to_file(tmp.path(), "100_spike_my_spike", "Third criterion")
+            .expect("add third criterion");
+
+        let contents = read_story_content(tmp.path(), "100_spike_my_spike").unwrap();
+        assert!(
+            contents.contains("## Acceptance Criteria"),
+            "AC section should be present"
+        );
+        assert!(
+            contents.contains("- [ ] First criterion"),
+            "first AC missing"
+        );
+        assert!(
+            contents.contains("- [ ] Second criterion"),
+            "second AC missing"
+        );
+        assert!(
+            contents.contains("- [ ] Third criterion"),
+            "third AC missing"
+        );
+    }
+
+    #[test]
+    fn update_story_acceptance_criteria_in_front_matter_returns_error() {
+        // Bug 625: passing acceptance_criteria via front_matter must return an
+        // explicit error rather than silently dropping the value.
+        let tmp = tempfile::tempdir().unwrap();
+        setup_story_in_fs(
+            tmp.path(),
+            "101_test",
+            "---\nname: T\n---\n\n## Acceptance Criteria\n\n- [ ] Existing\n",
+        );
+
+        let mut fields = HashMap::new();
+        fields.insert(
+            "acceptance_criteria".to_string(),
+            serde_json::json!(["crit 1", "crit 2"]),
+        );
+        let result = update_story_in_file(tmp.path(), "101_test", None, None, Some(&fields));
+        assert!(result.is_err(), "should fail with reserved-field error");
+        let err = result.unwrap_err();
+        assert!(
+            err.contains("acceptance_criteria"),
+            "error should name the reserved field: {err}"
+        );
     }
 
     // ── remove_criterion_from_file tests ──────────────────────────────────────