diff --git a/packages/core/src/prompter/example.ts b/packages/core/src/prompter/example.ts
new file mode 100644
index 0000000000..e38e8b5285
--- /dev/null
+++ b/packages/core/src/prompter/example.ts
@@ -0,0 +1,74 @@
+/**
+ * @license
+ * Copyright 2026 Google LLC
+ * SPDX-License-Identifier: Apache-2.0
+ */
+
+import { Prompt, prompt } from './prompter.js';
+
+// prompts can be functions that depend on context
+export const identity = prompt(
+  (ctx) =>
+    `You are Gemini CLI, an ${ctx.preamble?.interactive ? 'interactive' : 'autonomous'} CLI agent.`,
+);
+
+// or they can be objects representing an XML or Markdown section
+export const securityMandates = prompt({
+  tag: 'security',
+  attrs: { importance: 'MAXIMUM' },
+  content: 'Never log or commit secrets. Protect .env and .git folders.',
+});
+
+// they can compose together, with individual content parts resolving based
+// on context and not rendering if conditions aren't met
+export const subagents = prompt({
+  id: 'subagents',
+  heading: 'Available Subagents',
+  condition: (ctx) => (ctx.subAgents?.length ?? 0) > 0,
+  content: [
+    'Sub-agents are specialized expert agents. Each sub-agent is available as a tool of the same name. You MUST delegate tasks to the sub-agent with the most relevant expertise.',
+    {
+      tag: 'available_subagents',
+      content: (ctx) =>
+        ctx.subAgents?.map((s) => `- ${s.name}: ${s.description}`).join('\n') ||
+        '',
+    },
+  ],
+});
+
+export const emptySection = prompt({
+  heading: 'This Should Not Render',
+  content: '', // Empty content causes section to be skipped
+});
+
+const myPrompt = new Prompt(
+  identity,
+  {
+    id: 'general_guidance',
+    heading: 'General Guidance',
+    content: [
+      'The following sections tell you how to behave. ALWAYS FOLLOW.',
+      securityMandates,
+    ],
+  },
+  { heading: 'Stuff You Can Use', content: subagents },
+  emptySection,
+);
+
+// We can add new prompt elements dynamically
+myPrompt.add('Here is an added note.');
+
+// We can dynamically contribute to sections by ID, allowing for
+// post-facto composability when adding new features
+myPrompt.contribute({
+  general_guidance: 'Be nice to humans.',
+  subagents: 'Consider using the web_search subagent for recent info.',
+});
+
+//eslint-disable-next-line no-console
+console.log(
+  await myPrompt.render({
+    preamble: { interactive: true },
+    subAgents: [{ name: 'foo', description: 'does foo stuff' }],
+  }),
+);
diff --git a/packages/core/src/prompter/prompter.test.ts b/packages/core/src/prompter/prompter.test.ts
new file mode 100644
index 0000000000..0d099f44ba
--- /dev/null
+++ b/packages/core/src/prompter/prompter.test.ts
@@ -0,0 +1,162 @@
+/**
+ * @license
+ * Copyright 2026 Google LLC
+ * SPDX-License-Identifier: Apache-2.0
+ */
+
+import { describe, expect, it } from 'vitest';
+import { Prompt } from './prompter.js';
+
+describe('Prompt', () => {
+  it('renders a simple string', async () => {
+    const prompt = new Prompt('Hello world');
+    expect(await prompt.render({})).toBe('Hello world');
+  });
+
+  it('renders a function content resolving dynamically', async () => {
+    const prompt = new Prompt<{ name: string }>((ctx) => `Hello ${ctx.name}`);
+    expect(await prompt.render({ name: 'Alice' })).toBe('Hello Alice');
+  });
+
+  it('renders an array of contents', async () => {
+    const prompt = new Prompt(['Part 1', 'Part 2']);
+    expect(await prompt.render({})).toBe('Part 1\n\nPart 2');
+  });
+
+  it('renders a section with heading', async () => {
+    const prompt = new Prompt({
+      heading: 'My Section',
+      content: 'This is the body',
+    });
+    expect(await prompt.render({})).toBe('# My Section\n\nThis is the body');
+  });
+
+  it('renders a section with tag and attrs', async () => {
+    const prompt = new Prompt({
+      tag: 'foo',
+      attrs: { bar: 'baz' },
+      content: 'Hello',
+    });
+    expect(await prompt.render({})).toBe('<foo bar="baz">\nHello\n</foo>');
+  });
+
+  it('allows adding content via .add()', async () => {
+    const prompt = new Prompt('Original');
+    prompt.add('Added later');
+    expect(await prompt.render({})).toBe('Original\n\nAdded later');
+  });
+
+  it('conditionally omits rendering a section based on condition', async () => {
+    const prompt = new Prompt<{ shouldRender: boolean }>(
+      {
+        heading: 'Conditional',
+        condition: (ctx) => ctx.shouldRender,
+        content: 'This might not appear',
+      },
+      'Always appears',
+    );
+    expect(await prompt.render({ shouldRender: false })).toBe('Always appears');
+    expect(await prompt.render({ shouldRender: true })).toBe(
+      '# Conditional\n\nThis might not appear\n\nAlways appears',
+    );
+  });
+
+  it('conditionally omits rendering a section based on an async condition', async () => {
+    const prompt = new Prompt<{ shouldRender: boolean }>(
+      {
+        heading: 'Conditional',
+        condition: async (ctx) => ctx.shouldRender,
+        content: 'This might not appear',
+      },
+      'Always appears',
+    );
+    expect(await prompt.render({ shouldRender: false })).toBe('Always appears');
+    expect(await prompt.render({ shouldRender: true })).toBe(
+      '# Conditional\n\nThis might not appear\n\nAlways appears',
+    );
+  });
+
+  it('allows dynamic contributions via .contribute()', async () => {
+    const prompt = new Prompt(
+      {
+        id: 'target',
+        heading: 'Target Section',
+        content: ['Initial content'],
+      },
+      {
+        id: 'other',
+        content: 'Other content',
+      },
+    );
+
+    prompt.contribute({
+      target: 'Contributed content',
+      missing: 'Should be ignored',
+    });
+
+    const result = await prompt.render({});
+    expect(result).toBe(
+      '# Target Section\n\nInitial content\n\nContributed content\n\nOther content',
+    );
+  });
+
+  it('converts single content into an array when contributing', async () => {
+    const prompt = new Prompt({
+      id: 'target',
+      heading: 'Target Section',
+      content: 'Initial content', // String, not array
+    });
+
+    prompt.contribute({
+      target: 'Contributed content',
+    });
+
+    const result = await prompt.render({});
+    expect(result).toBe(
+      '# Target Section\n\nInitial content\n\nContributed content',
+    );
+  });
+
+  it('skips rendering headings and tags if the content is empty', async () => {
+    const prompt = new Prompt(
+      {
+        heading: 'Empty Section',
+        tag: 'empty',
+        content: '', // Empty string
+      },
+      {
+        heading: 'Empty Array Section',
+        content: [], // Empty array
+      },
+      {
+        heading: 'Function resolving to empty',
+        content: () => '',
+      },
+      'Visible content',
+    );
+
+    expect(await prompt.render({})).toBe('Visible content');
+  });
+
+  it('handles nested structures properly in contribute', async () => {
+    const prompt = new Prompt({
+      heading: 'Outer',
+      content: [
+        {
+          id: 'inner',
+          heading: 'Inner',
+          content: 'Inner content',
+        },
+      ],
+    });
+
+    prompt.contribute({
+      inner: 'Injected into inner',
+    });
+
+    const result = await prompt.render({});
+    expect(result).toBe(
+      '# Outer\n\n## Inner\n\nInner content\n\nInjected into inner',
+    );
+  });
+});
diff --git a/packages/core/src/prompter/prompter.ts b/packages/core/src/prompter/prompter.ts
new file mode 100644
index 0000000000..3b336d2b71
--- /dev/null
+++ b/packages/core/src/prompter/prompter.ts
@@ -0,0 +1,139 @@
+/**
+ * @license
+ * Copyright 2026 Google LLC
+ * SPDX-License-Identifier: Apache-2.0
+ */
+
+import type { SystemPromptOptions } from 'src/prompts/snippets.js';
+import type { PromptContent, PromptSection } from './types.js';
+
+// Helper to stringify XML attributes cleanly
+function renderAttributes(attrs?: Record<string, string>): string {
+  if (!attrs) return '';
+  return Object.entries(attrs)
+    .map(([key, value]) => ` ${key}="${value}"`)
+    .join('');
+}
+
+export class Prompt<C = SystemPromptOptions> {
+  private contents: Array<PromptContent<C>>;
+
+  constructor(...contents: Array<PromptContent<C>>) {
+    this.contents = contents;
+  }
+
+  add(content: PromptContent<C>): void {
+    this.contents.push(content);
+  }
+
+  contribute(contributions: Record<string, PromptContent<C>>): void {
+    const traverse = (node: PromptContent<C>) => {
+      if (Array.isArray(node)) {
+        node.forEach(traverse);
+      } else if (typeof node === 'object' && node !== null) {
+        // In this branch, node is a PromptSection<C>
+        const section = node;
+        const contribution = contributions[section.id ?? ''];
+        if (section.id && contribution) {
+          const content = section.content;
+          if (Array.isArray(content)) {
+            content.push(contribution);
+          } else {
+            section.content = [content, contribution];
+          }
+        }
+        traverse(section.content);
+      }
+    };
+
+    this.contents.forEach(traverse);
+  }
+
+  async render(context: C, options?: { depth?: number }): Promise<string> {
+    const parts = await Promise.all(
+      this.contents.map((item) => Prompt.renderContent(context, item, options)),
+    );
+    return parts.filter((part) => part.length > 0).join('\n\n');
+  }
+
+  private static async renderContent<C>(
+    context: C,
+    content: PromptContent<C>,
+    options?: { depth?: number },
+  ): Promise<string> {
+    // 1. if function: run function with context and process result
+    if (typeof content === 'function') {
+      const resolved = await content(context);
+      // keep passing options down so depth isn't lost
+      return Prompt.renderContent(context, resolved, options);
+    }
+
+    // 2. if string: simple string append
+    if (typeof content === 'string') {
+      return content;
+    }
+
+    // 3. if array: process and concatenate each item in the array
+    if (Array.isArray(content)) {
+      const parts = await Promise.all(
+        content.map((item) => Prompt.renderContent(context, item, options)),
+      );
+      // Filter out empty strings to prevent huge gaps, then separate with double newline
+      return parts.filter((part) => part.length > 0).join('\n\n');
+    }
+
+    // 4. if object: process as section
+    if (typeof content === 'object' && content !== null) {
+      if (content.condition) {
+        const shouldRender = await content.condition(context);
+        if (!shouldRender) {
+          return '';
+        }
+      }
+      return Prompt.renderSection(context, content, options);
+    }
+
+    return '';
+  }
+
+  private static async renderSection<C>(
+    context: C,
+    section: PromptSection<C>,
+    options?: { depth?: number },
+  ): Promise<string> {
+    const depth = options?.depth ?? 1;
+    // Standard Markdown headings max out at h6 (######)
+    const headingLevel = Math.min(depth, 6);
+
+    // Pass context and increment depth for nested sections
+    // section.content is an array, which renderPrompt already knows how to handle
+    const innerContent = await Prompt.renderContent(context, section.content, {
+      depth: depth + 1,
+    });
+
+    if (!innerContent) {
+      return '';
+    }
+
+    let result = '';
+
+    if (section.heading) {
+      result += `${'#'.repeat(headingLevel)} ${section.heading}\n\n`;
+    }
+
+    if (section.tag) {
+      const attrs = renderAttributes(section.attrs);
+      result += `<${section.tag}${attrs}>\n${innerContent}\n</${section.tag}>`;
+    } else {
+      result += innerContent;
+    }
+
+    return result.trim();
+  }
+}
+
+export function prompt(
+  content: PromptContent<SystemPromptOptions>,
+): PromptContent<SystemPromptOptions> {
+  return content;
+}
diff --git a/packages/core/src/prompter/types.ts b/packages/core/src/prompter/types.ts
new file mode 100644
index 0000000000..84a6f01c48
--- /dev/null
+++ b/packages/core/src/prompter/types.ts
@@ -0,0 +1,31 @@
+/**
+ * @license
+ * Copyright 2026 Google LLC
+ * SPDX-License-Identifier: Apache-2.0
+ */
+
+export type ContextResolver<C, O> = O | ((ctx: C) => O | Promise<O>);
+
+export type PromptSection<C> = {
+  /** Unique identifier for the section if it can receive contributions. */
+  id?: string;
+  /** Add a Markdown heading of appropriate level to this section. */
+  heading?: string;
+  /** If supplied, wrap this section in an XML tag. */
+  tag?: string;
+  /** If supplied, add attributes to the XML section tag. */
+  attrs?: Record<string, string>;
+
+  /** Condition that must evaluate to true for the section to be rendered. */
+  condition?: (ctx: C) => boolean | Promise<boolean>;
+
+  // Notice we use the generic <C> here so the children know about the context
+  content: PromptContent<C>;
+};
+
+// The core recursive type.
+// It wraps your 3 base node shapes (string, section, or array) in the resolver.
+export type PromptContent<C> = ContextResolver<
+  C,
+  string | PromptSection<C> | Array<PromptContent<C>>
+>;