diff --git a/ui/goose2/src/features/projects/lib/projectPromptText.test.ts b/ui/goose2/src/features/projects/lib/projectPromptText.test.ts
index a66371fc71..881a13a336 100644
--- a/ui/goose2/src/features/projects/lib/projectPromptText.test.ts
+++ b/ui/goose2/src/features/projects/lib/projectPromptText.test.ts
@@ -19,38 +19,56 @@ describe("projectPromptText", () => {
     });
   });
 
-  it("keeps blank lines between include lines and prompt content", () => {
+  it("places includes after the prompt text", () => {
+    expect(buildEditorText(["/tmp/one"], "My prompt")).toBe(
+      "My prompt\n\ninclude: /tmp/one",
+    );
+  });
+
+  it("handles includes-only text (no prompt)", () => {
+    expect(buildEditorText(["/tmp/one", "/tmp/two"], "")).toBe(
+      "include: /tmp/one\ninclude: /tmp/two",
+    );
+  });
+
+  it("collects include lines from anywhere in the editor text", () => {
     expect(
-      parseEditorText("include: /tmp/one\n\ninclude: /tmp/two\nprompt"),
+      parseEditorText("include: /tmp/one\nprompt\n\ninclude: /tmp/two"),
     ).toEqual({
       prompt: "prompt",
       workingDirs: ["/tmp/one", "/tmp/two"],
     });
   });
 
-  it("keeps include-looking prompt lines after prompt content begins", () => {
+  it("treats trailing include lines as working directories when saving", () => {
     expect(parseEditorText("prompt first\ninclude: /tmp/kept")).toEqual({
-      prompt: "prompt first\ninclude: /tmp/kept",
-      workingDirs: [],
+      prompt: "prompt first",
+      workingDirs: ["/tmp/kept"],
     });
   });
 
-  it("creates a leading include block for prompt-only text", () => {
+  it("creates a trailing include block for prompt-only text", () => {
     expect(insertWorkingDir("Existing prompt", "/tmp/one")).toBe(
-      "include: /tmp/one\n\nExisting prompt",
+      "Existing prompt\n\ninclude: /tmp/one",
     );
   });
 
-  it("appends a directory within the leading include block", () => {
+  it("appends a directory to the trailing include block", () => {
     expect(
-      insertWorkingDir("include: /tmp/one\n\nPrompt body", "/tmp/two"),
-    ).toBe("include: /tmp/one\ninclude: /tmp/two\n\nPrompt body");
+      insertWorkingDir("Prompt body\n\ninclude: /tmp/one", "/tmp/two"),
+    ).toBe("Prompt body\n\ninclude: /tmp/one\ninclude: /tmp/two");
+  });
+
+  it("adds a new directory to the bottom without moving existing prompt text", () => {
+    expect(insertWorkingDir("include: /tmp/one\nPrompt body", "/tmp/two")).toBe(
+      "include: /tmp/one\nPrompt body\n\ninclude: /tmp/two",
+    );
   });
 
   it("treats tilde and absolute paths as equivalent when checking duplicates", () => {
     expect(
       hasEquivalentWorkingDir(
-        "include: ~/dev/goose2\n\nPrompt body",
+        "Prompt body\ninclude: ~/dev/goose2",
         "/Users/mtoohey/dev/goose2",
         "/Users/mtoohey",
       ),
@@ -60,7 +78,7 @@ describe("projectPromptText", () => {
   it("does not match different directories when checking duplicates", () => {
     expect(
       hasEquivalentWorkingDir(
-        "include: ~/dev/goose2\n\nPrompt body",
+        "Prompt body\ninclude: ~/dev/goose2",
         "/Users/mtoohey/dev/other",
         "/Users/mtoohey",
       ),
@@ -70,7 +88,7 @@ describe("projectPromptText", () => {
   it("treats trailing slashes as equivalent when checking duplicates", () => {
     expect(
       hasEquivalentWorkingDir(
-        "include: /Users/mtoohey/dev/goose2/\n\nPrompt body",
+        "Prompt body\ninclude: /Users/mtoohey/dev/goose2/",
         "/Users/mtoohey/dev/goose2",
         "/Users/mtoohey",
       ),
diff --git a/ui/goose2/src/features/projects/lib/projectPromptText.ts b/ui/goose2/src/features/projects/lib/projectPromptText.ts
index 182fe704b0..5c65e83cbb 100644
--- a/ui/goose2/src/features/projects/lib/projectPromptText.ts
+++ b/ui/goose2/src/features/projects/lib/projectPromptText.ts
@@ -4,12 +4,13 @@ import { INCLUDE_RE } from "./includePattern";
 export function buildEditorText(workingDirs: string[], prompt: string): string {
   const includeLines = workingDirs.map((directory) => `include: ${directory}`);
   if (includeLines.length === 0) return prompt;
-  return [...includeLines, "", prompt].join("\n");
+  if (prompt === "") return includeLines.join("\n");
+  return [prompt, "", ...includeLines].join("\n");
 }
 
 /** Parse editor text into { prompt, workingDirs }.
- *  Only `include:` lines at the top of the text (before the first
- *  non-include, non-blank line) are treated as working directories. */
+ *  `include:` lines can appear anywhere in the editor text and are
+ *  extracted into workingDirs when the project is saved. */
 export function parseEditorText(text: string): {
   prompt: string;
   workingDirs: string[];
@@ -17,26 +18,21 @@ export function parseEditorText(text: string): {
   const lines = text.split("\n");
   const workingDirs: string[] = [];
   const promptLines: string[] = [];
-  let parsingIncludeBlock = true;
 
   for (const line of lines) {
     const match = line.match(INCLUDE_RE);
-    if (parsingIncludeBlock && match) {
+    if (match) {
       workingDirs.push(match[1].trim());
       continue;
     }
 
-    if (line.trim() !== "") {
-      parsingIncludeBlock = false;
-    }
-
     promptLines.push(line);
   }
 
+  // Trim leading/trailing blank lines from the prompt.
   while (promptLines[0]?.trim() === "") {
     promptLines.shift();
   }
-
   while (promptLines[promptLines.length - 1]?.trim() === "") {
     promptLines.pop();
   }
@@ -48,12 +44,17 @@ export function parseEditorText(text: string): {
 }
 
 export function insertWorkingDir(text: string, directory: string): string {
-  if (text === "") {
+  const trimmedText = text.trimEnd();
+
+  if (trimmedText === "") {
     return `include: ${directory}`;
   }
 
-  const { prompt, workingDirs } = parseEditorText(text);
-  return buildEditorText([...workingDirs, directory], prompt);
+  const trimmedLines = trimmedText.split("\n");
+  const lastLine = trimmedLines[trimmedLines.length - 1] ?? "";
+  const separator = lastLine.match(INCLUDE_RE) ? "\n" : "\n\n";
+
+  return `${trimmedText}${separator}include: ${directory}`;
 }
 
 export function hasEquivalentWorkingDir(