diff --git a/.github/workflows/generate-docs.yml b/.github/workflows/generate-docs.yml
index 8b68c8b2..cfc1ee37 100644
--- a/.github/workflows/generate-docs.yml
+++ b/.github/workflows/generate-docs.yml
@@ -21,7 +21,11 @@ on:
 env:
   DOCS_TOKEN: ${{ secrets.DOCS_TOKEN }}
   TARGET_REPOSITORY: OctopusDeploy/docs
-  TARGET_DIRECTORY: src/pages/docs/octopus-rest-api/cli
+  # The command pages. _generated is the docs repo's convention for a folder a
+  # generator owns outright, served from the folder above it by an Astro route.
+  TARGET_DIRECTORY: src/pages/docs/cli/_generated
+  # The rows the hand-written overview page at /docs/cli imports.
+  COMMAND_LIST_PATH: src/shared-content/cli/commands.include.md
   # Always sync to the same branch in case there's already an open PR, in which case it'll be updated
   SYNC_BRANCH: cli-docs-sync
   PR_LABEL: cli-docs-sync
@@ -56,7 +60,13 @@ jobs:
 
       - name: Generate cli docs
         working-directory: cli
-        run: mkdir -p ../docs/$TARGET_DIRECTORY && go run cmd/gen-docs/main.go --website --doc-path ../docs/$TARGET_DIRECTORY --relative-base-path /docs/octopus-rest-api/cli
+        run: |
+          mkdir -p ../docs/$TARGET_DIRECTORY
+          go run cmd/gen-docs/main.go \
+            --website \
+            --doc-path ../docs/$TARGET_DIRECTORY \
+            --command-list-path ../docs/$COMMAND_LIST_PATH \
+            --relative-base-path /docs/cli
 
       - name: Commit and push
         id: commit
@@ -69,10 +79,10 @@ jobs:
           git config user.email 'bob@octopus.com'
           git config user.name octobob
 
-          git add --all -- "$TARGET_DIRECTORY"
+          git add --all -- "$TARGET_DIRECTORY" "$COMMAND_LIST_PATH"
 
-          # Safety net: only the target folder should have been touched
-          unexpected_changes="$(git diff --cached --name-only -- . ":(exclude)$TARGET_DIRECTORY")"
+          # Safety net: only the generated files should have been touched
+          unexpected_changes="$(git diff --cached --name-only -- . ":(exclude)$TARGET_DIRECTORY" ":(exclude)$COMMAND_LIST_PATH")"
           if [ -n "$unexpected_changes" ]; then
             echo "Found unexpected staged changes, aborting" >&2
             echo "$unexpected_changes" >&2
diff --git a/cmd/gen-docs/main.go b/cmd/gen-docs/main.go
index bccfe691..684c7dbd 100644
--- a/cmd/gen-docs/main.go
+++ b/cmd/gen-docs/main.go
@@ -83,6 +83,7 @@ func run(args []string) error {
 	website := flags.BoolP("website", "", false, "Generate website pages")
 	dir := flags.StringP("doc-path", "", "", "Path directory where you want generate doc files")
 	relativeBasePath := flags.StringP("relative-base-path", "", "", "Relative base path for generating index links")
+	commandListPath := flags.StringP("command-list-path", "", "", "File to write the command list include to. Skipped when unset")
 	help := flags.BoolP("help", "h", false, "Help about any command")
 
 	if err := flags.Parse(args); err != nil {
@@ -127,17 +128,39 @@ func run(args []string) error {
 			return err
 		}
 
-		filename := filepath.Join(*dir, "index.md")
-		f, err := os.Create(filename)
+		written := make(map[string]bool, pageCollection.Pages.Len())
+		for _, page := range *pageCollection.Pages {
+			written[filepath.Base(page.OutputFile)] = true
+		}
+
+		// A generator failure that produced almost nothing would otherwise sync as
+		// a mass deletion. The real count is in the hundreds.
+		if len(written) < minimumPageCount {
+			return fmt.Errorf("only generated %d page(s), expected at least %d, so something went wrong", len(written), minimumPageCount)
+		}
+
+		if err := pruneStalePages(*dir, written); err != nil {
+			return err
+		}
+
+		if *commandListPath == "" {
+			return nil
+		}
 
+		if err := os.MkdirAll(filepath.Dir(*commandListPath), 0755); err != nil {
+			return err
+		}
+
+		// Not `f`: that is the command factory, several lines up.
+		out, err := os.Create(*commandListPath)
 		if err != nil {
 			return err
 		}
-		defer f.Close()
-		t := template.Must(template.New("index-template").Parse(indexTemplate))
+		defer out.Close()
+
 		sort.Sort(pageCollection.Pages)
-		t.Execute(f, pageCollection)
-		return nil
+		t := template.Must(template.New("command-list-template").Parse(commandListTemplate))
+		return t.Execute(out, pageCollection)
 	}
 
 	header := &doc.GenManHeader{
@@ -154,6 +177,32 @@ func run(args []string) error {
 	return nil
 }
 
+// Below this, assume the generator broke rather than that the CLI lost most of
+// its commands.
+const minimumPageCount = 50
+
+// pruneStalePages removes the .mdx files in dir that this run did not write, so
+// a renamed or removed command takes its page with it.
+func pruneStalePages(dir string, written map[string]bool) error {
+	entries, err := os.ReadDir(dir)
+	if err != nil {
+		return err
+	}
+
+	for _, entry := range entries {
+		name := entry.Name()
+		if entry.IsDir() || filepath.Ext(name) != ".mdx" || written[name] {
+			continue
+		}
+		if err := os.Remove(filepath.Join(dir, name)); err != nil {
+			return err
+		}
+		fmt.Fprintf(os.Stderr, "removed stale page %s\n", name)
+	}
+
+	return nil
+}
+
 func GenMarkdownCustom(cmd *cobra.Command, w io.Writer, info *TemplateInformation) error {
 	cmd.InitDefaultHelpCmd()
 	cmd.InitDefaultHelpFlag()
@@ -214,7 +263,7 @@ func contentEqualIgnoringModDate(a, b []byte) bool {
 }
 
 const documentationTemplate = `---
-layout: src/layouts/Default.astro
+layout: src/layouts/Cli.astro
 pubDate: 2023-01-01
 modDate: {{.Date}}
 title: {{.Title}}
@@ -263,32 +312,12 @@ Use "{{.CommandPath}} [command] --help" for more information about a command.{{e
 
 ## Learn more
 
-- [Octopus CLI](/docs/octopus-rest-api/cli)
+- [Octopus CLI](/docs/cli)
 - [Creating API keys](/docs/octopus-rest-api/how-to-create-an-api-key)
 `
 
-const indexTemplate = `---
-layout: src/layouts/Default.astro
-pubDate: 2023-01-01
-modDate: 2023-01-01
-title: CLI
-description: The all-new Octopus CLI
-navOrder: 100
-hideInThisSection: true
----
-
-The Octopus CLI is a command line tool that builds on top of the [Octopus Deploy REST API](/docs/octopus-rest-api). With the Octopus CLI you can push your application packages for deployment as either Zip or NuGet packages, and manage your environments, deployments, projects, and workers.
-
-The Octopus CLI can be used on Windows, Mac, Linux and Docker. For installation options and direct downloads, visit the [CLI Readme](https://github.com/OctopusDeploy/cli/blob/main/README.md).
-
-:::div{.hint}
-The Octopus CLI is built and maintained by the Octopus Deploy team, but it is also open source. You can [view the Octopus CLI project on GitHub](https://github.com/OctopusDeploy/cli), which leans heavily on the [go-octopusdeploy library](https://github.com/OctopusDeploy/go-octopusdeploy).
-:::
-
-## Commands {#octopusCommandLine-Commands}
-
-` + "`octopus` supports the following commands:" +
-	`
-{{range .Pages}}
-- **[{{.Title}}]({{.RelativePath}})**:  {{.Command.Short}}.{{end}}
-`
+// The rows the overview page lists. The prose around them, and the frontmatter,
+// belong to the docs repo: this is imported by src/pages/docs/cli/index.mdx as a
+// shared-content include, so a wording change there needs no release here.
+const commandListTemplate = `{{range .Pages}}- **[{{.Title}}]({{.RelativePath}})**:  {{.Command.Short}}.
+{{end}}`